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Volume 93, Number 1 
May 2006 

Annals of the 

Missouri Botanical Garden 


The Annals, published quarterly, contains papers, primarily in systematic botany, 
contributed from the Missouri Botanical Garden, St. Louis. Papers originaling outside 
the Garden will also be accepted. All manuscripts are peer-reviewed by qualified, 
independent reviewers. Authors should write the Managing Editor for information 
concerning arrangfnnents for pu])llshing in the Annai.s. Instructions to Authors are 
printed in the back of the last issue of each voluin(^ and are also available online at 
www. mligpres s .org. 


Editorial Coiiiinittee 

Victoria C. Hollowell 
Scienufic Editor^ 

Missouri Botanical Garden 

Belli Parada 
Managing Editor^ 

Missouri Botanical Garden 

Diana Guiiter 

Associate Editor^ 
Missouri Botanical Garden 

Barbara Mack 

Editorial Assistant^ 
Missouri Botanical Garden 

Adele Niblack 
MBG Press Assistant, 
Missouri Botaniccd Garden 

Ihsaii A. Al-Sliehl)az 
Missouri Botanical Garden 

Gerril Davidse 

Missouri Botanical Garden 

Roy E, Gereau 

Missouri Botanical Garden 

Peter Goldhlalt 

Missouri Botanical Garden 

Goidon McPherson 
Missouri Botanical Garden 

R Mick Richardson 

Missouri Botanical Garden 

Charlolte Taylor 
Missouri Botanical Garden 

Henk van der Werff 
Missouri Botanical Garden 






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6 2006 


of th 









1, 2 

P. Mick Richardson^ 


The Annual Systematics Symposium that took place In order to bring attention to a display of Linnaean 

at the Missouri Botanical Garden in 2003 marked material in the Monsanto Research Building, the ne^\ 

a major milestone in the histor}^ of scientific discourse location of the library, a Special Linnaean Celebration 

in the U.S.A. The Systematics Symposium is remark- Talk was aiTanged on the Friday evening, an atypical 

able for its unbroken run of 50 years at the same time for one of our symposium talks. This was 

institution. Also noteworthy is the fact tliat the delivered by Mar}^ P. ('Tolly^') Winsor. Although it 

National Science Foundation has supported 48 of is pul)lished here with the succinct title ''Linnacus's 

the symposia. What is the explanation for such a long biology was not essentialist," it was advertised and 

run of successful symposia, and why does each delivered with the intriguing title "Would you like 

symposium continue to 

fill the seats of a large your species concept rare, sir, or well-done? (A look at 

auditorium? Certainly, some of the audience comes how the histor)^ of science is cooked, how you can tell, 
for an annual visit to the massive herbarium or the and whether it is any good for you anyway)." The room 

comprehensive library, to visit a 1 

arge city 

for was filled to overflowing, and especially notable in 

shopping, or for the chance of an exotic meal, but the audience were the local histor)^ of science pro- 
most of the audience come to hear the symposium fessionals, a group not always seen at the symposium. 

speakers. There is a distinct freshness to each 

Saturday, as usual, was the main day of the 

symposium because eveiy year the list of speakers is symposium. Jonatlian Loses moderated the morning 

chosen by a new set of organizers. This year was no session, and Peter Stevens was the afternoon moder- 

exception, and the organizers comprised a zoologist ator. Peter Raven introduced the evening speakers, 

and a botanist. Jonathan Losos and Peter Stevens a husband and wife team of scientists. All but one of 

invited a diverse group of speakers to shed some light the speakers has submitted a manuscript in time for 

on the perennial subject of "the species question. 


publication here. 

^This and ihc seven articles that follow it are the proceedings of the 50th Annual Systematics Symposium of the Missom-i 
Botanical Garden, Species Reconsidered: Consequences for Biodiversity and Evolution. The symposium was held 10-11 October, 
2003, at the Missouri Botanical Garden in St. Louis, Missouri, U.S.A. 

The symposium was supported in part by the National Science Foundation under grant DEB-9981642. I thank Jonathon 
Losos and teeter Stevens for selecting an interesting diversity of speakers. 1 also thank Sandy Popez and Maiy McNamara for 
their dedicated organizational and administrative assistance, Maiy Merello and Amy Pool for their help with the registration 
process, and Alina Freire-Fierro for her expertise in producing the symposium booklet and getting the information onto the 
Garden website in a timely fashion. Past hut not least, T wish to thank the speakers for making the symposium so wonderfully 


^The editors of the Annals thank Sophia Btrlcomh for her editorial contribution to these papers. 
^'Missouri Botanical Garden, P.O. Box 299, St. L)uis Missouri 63166, U.S.A. 

Ann. Missouri Bot. Gaud. 93: 1. Pubijshed on 31 May 2006. 


Mary l\ Winsor- 


The curriiil [ilrlurc of the 1ii>1(H) uf taxoiuuii) iiu-nrporatcs A. J. CaiiiV claim thai Liimarus stm\e In appiv ihc logical 
mclliod o! (Icfinill(in taughl h) rntMli<-val fulloucrs of Arl^lotle. Cain's ar^^LiiiicuL does not slaiitl up lo crilical cxaniiiiation. 
Contrary lo some piihiished slatrrnenis, thtu'c is no evid(^nce thai riiina^-us ever studied lo^ic. His use of die wortis ''genus'" 
and ''species" mined the meauiii<; diey had in lo<^ic. ;uid ''essentiar* tneatil lo him nicivly 'Maxononiieally usehd." The 
essenlialisni slory, a narrative dial has most pre-Darwinian hiologists sl<'eped in die worhl \ iew rtf Plalf) and \risto[|c. is ill- 
fou tided anil i[]ipi()ha])h\ 

Key liorfls: A.J, CaiiL essetilialisnu liist()i-\ of s\ slenialies, l]i^lor\ of la\<aiomv. I.iniiacus. E. Ma\r. 

Thi; Missiiiiri Bolaniedl Cafdcii lias celehralcd the 

ihe ntaliii-e l.jnnaeus ihitik that sonic sj)e('jes were 

25()th anniversary of the pul)li('alion of Liiuiaeus's created with an inintulahle essence and ollicrs with 
Species Planliuum (Linnaeus. 1 7o3). hti( there are miilahle essences? Ernst M^ 


douhness some hiologists who are not stn'c if LJ 

\\v nescr\"es crec 

lit f 

stn-e il LJicy are a(huitlin<i the proljlem (1982: 239). hul lie h^ives us h) 
proud of ihal landmark. After all, we have now con(dude tliat Linnaeus was ]iopelessly confnscfl and 

inconsislcid. I sug^^esl llial il is we wlio arc confused, 
for we athlhute to IJnnaeus a philosophical nntion he 

departed so far from tlic l)cli(ds of that eccentric ohi 
Swede that it is rather eniharrassing to couul htm 
among our Inhdlectual ancesU)rs. Didn't he think thai 
eveiy species w^as directly created hy God, in cdicr 

nc\ cr 


ActualL . 1 snsi^ect that mativ of us are allnwinu' me 

words, wasnT he a creationist and thus an entauy of spectre of modern crealionism to bias our nndcisland- 

evolution? More profoundly, dlfhi'l Linnaeus l)(di(ne ing of a prc-Danvinian creationist like Litinaeiis. To 

that every s])(x;ies has its own essence, that is, l\i)c in 

the Phitonic sense? Well, to he Muni, no, and no. Mis 

views on the fixity of >pecies (dianged in his lifetime, the essetilialism stor\ s(M'Tn plausible, but the link 

and the ])iisiness about essetilialism is the scdiolarly cotmcctiuii; these realms was the iiisi<ihl of a later 

a modern biologist who does not bclitnc in God, 
Linnaeus's explicit piety lias the effect of making 

cqui\alenl of an urban myth, ihal is, a story everyone general ion, Tn 1857 Louis Agassiz, disliuLed by the 

repeals btil lor which theiv is scant basis iti fact. rising interest in evolution, argued in his ^^Essay on 

Thai the mature Linnaeus al)andoned his yontlifn! Classification" that ihe Creator had coiicei\(Ml each 

insistence on the fixity of s[)ecies was pointed onl by species in his divini; itit(dK;cl before gi\dng it material 

Edw^ard Greene (1909) and lully documented ])\ John existence (W insor, 1991). lb- repeated tjiese ideas 

Ramsboltom (1938). Linnaeus was perfectly cotnfort- afh-r Darwin's revolulionary book a|-)|)earcHl In 1859, 

able imagining that God may have made, in lbs and Agassiz remaincMl adatnant thai the pallerns 

one species per recorded by taxonomists were direct e\ idencc of God's 

genus, while natural proc-esses later caused the thoughts. But all this was a century after Linnaeus. In 
emergence of the others. Although it is verv \\v 
ktiown that Linnaeus underwent this shift from 

original luu-st of creatixity, only 

Linnaeus's day the "refjuirement- of Christian faith," 
contrary to Mayr's claim (1982: 259), did not forbid 
absolute fixity lo liniil(Ml Iransinutatiou (Larson, the possibility thai the '■kinds'^ mentioned in tlu^ Book 
1971; Koeruer, 1999; MiilhM--\Ville, 1999), 1 remitid of Genesis could have l)C(ai at the tcixonomists^ rank of 
you ol il because il so clear]} contradicts the utLan 
myth abtnit essentialism. d1ic whole point about xvho do b(dieve in God A\ill lia\c more sympathv with 
Platonic types, we have bccti lold time and again, is Liunaiar-^ than with Agassi/, because they accept that 
that there arc inibridgcable ga|ts separating them. Did the Creator willed into existence om" actual world. 

genus rather \\vc 

in sj)ecies 

. Those modern biologists 

' My reseaivli was supported h\ a gratit from the Social Sciences and Humanities Rest^areh (Council of ('anada. for which I 

am veiT gratehil. I'or their assistance and encouragement 1 also tliatik Strphan Multer-Vidlle and mv students Ahhy Slinger. 

Jennder llert/, Klise Paradis, and Dennis Yeiing. I am iiartieularly indehted to Peter St<'\ens and Peter Raven for in\ iling me 

to the \bssouM Hotanieal Larden"^ oOth Annu;il Systeniaties Symp()>!imi, and 1 thank MitL Rieliardson for arrau;iiui; such 
a pleasant \ i^il. 

^lu^tilute lor the I rh-.tory and Philosophy of Science and Technology. Victoria College, Ihiiversitv of Ton 
Park Creseetil East. Tofonlo, Otilario M5S I ]<:7, Canada, polly.u iti^or(?uIoronlo.(;a. 



into. (■> »^/neeii s 

Ann. Missoriii Box. Gaud. 93: 2-7. Pi hiimifd on 31 Ma^ 2006. 

Volume 93, Number 1 

Linnaeus's Biology 


including life with all its evolutionary complexity and 
history. Those biologists realize thai belief in God 
does not logically entail belief in tlu^ fixity of species. 

The mature Linnaeus's limited transmutation was. 


Mayr (19<)2: 259) admits, "not only inconsistent will 
eventhing he had said and believed l)(Torc but was in 
fact irreconcilable with essentialism." \\ is time, iIkmi, 
to look more carefully at this supposed doctrine or 
dojrma of essentialism. Without a doubt, there does 
exist tochiy a story about essentialist beliefs in past 
centuries. It is this story, tliat is, this Instorical claim 
about the world-view^ of [tast taxonomists, that I am 
challenging. (Some philosophers are now refur])ishn]g 

Lriauglc. And so it is with liorses, or any other species: 
each lias an etenial, iniiiiu table essence, but each 
indi\idual has imperfections. In [his ])hilosophy of 
KSSKNTIALISM, variation is ciccidental imperfection; only 
essences matter. 

Plato's philosophy of essentialism Ix^eame incorporated 
into Western philosophy. Its cent ml tenet was that 
however nuu^h the objects in a class might accidcnUilly 
vary, lUc tdass still liad a defining essence tliat could not 
change. Tluis each spcc-ies — horse, zebra, or ass, for 
instance — has an essence, and one cannot be changed 
into another any more llian a triangle can vaiy enough to 
become a rectangle. 

The chief source of this historical naiTative is Ernst 

the word essentialism for variously moderni/ed Mayr (1059, 1963, 1968, 1976, 1982), whose words 

concepts of natural kijids, but the biological and 

have carried such authoritv that his claims Iiave been 

historical literature to which I refer was innocent ol rarely qm^stioned. Yet in its broad sweep across the 

such sophistication. Whether concepts of natural history of systematics, this story is not merely 

kinds corresponding to such 21st century usage were Inaccurate in particulars, it is wrong and harmful in 

held in the past is an entirely separate rpiestion not its Ixisic message. According to th(^ essentialism story, 

relevant here [Boyd, 1999: 152; Ellis, 2002].) 1 begin Plat(uiic idealism dominated Western thought until 

by laying before you only one telling of the Darwin broke its spell, whereas in fad, William of 

essentialism stoiy, but it stands for other repetitions Ockham in the llth century and other nominalists 

that luunber in the thousands, if we Include un- deah it crushing blows from which it tiever recovered, 

dergraduate lectures. Tlu^ latest edition of one of ihc Systematic biology evolved, largely independent of 

most widely used textbooks, Evolutionary Biology by philoso[)liy, from the 16th century onward, through 

Futuyma (1998: 448), puts it this way: 

Linnaeus and other early taxonomists held what t'rnsl 
Mayr (1942, 1963)-' has called a "TYPoroGtCAi " or 

"l^SSKNTtAi.lST" XOTlONOKSt'ECIES. lodividnals were members 

of a given species if they sufficiently conformed to lliat 
"t\i)e," or ideal, in certain characters tliat wta'c 

the actions of an army of herbalists, encyclopedists, 

of collections, and other 

makers and cataloguers 


Plato's 'Ideas" (see chapter 1). 

naturalists, whose joint efforts built up the mountain 
of data that Linnaeus confronted. None of Linnaeus's 
numerous enemies noticed any renmant of Plato's 
ideal forms in the series of catalogues the Swedish 

essential" fixed proitcrtics — a conce[)t descended from professor and his followers kt^pt cluu-ning out. Quite 

the coutraiy, one philosopher later noted with surprise 
and respect that naturalists' success in their massive 
project of inventory seemed to involve an active 
neglect of the classic niles of logical definition 
(WhewelL 1847; W^insur, 2003). B) suppressing tins 
rich history, the essentialism stor}^ distorts the 
historical and logical foimdation of Danvinism. 

To fidly understand llie creation antl impact of the 
essentiabsui stoi*} would require us to take it apart 

Here are the relevant passages in his chapter 1 
(Futuyma 1998: 6): 

In positing an evolutionary process wlierein natuial 
selection sorts among hereditary vailallons, Danrin 
identifiod niriation as a centrally Important Jact of 
biological sysfems. In doing so, he broke whh a 2()00- 
year-old tradition thai had dominated W estern thou<;lit. 

The tradition stemmed from Plato, whose phdosophy was , . . . , -_ ■, .-,,,^^^.,1 T ,.,:U 

, ., , r I u ■ 1 - 1 ../ - .. ! - tmd examme it uu^cc by piece, t)ut at piesent t wili 

built on the eoncepi ol Itie euios, llic lorm or idea, 1 i - i t • 1 • ir 

a transcendent ideal fomi imperfectly nnitated by its li^^^i' "ly attention to the claim that Lmnaeus himself 

earthly representations. In his famons metaphor of the was in duall to this philosophy. Mayr's sources for this 

cave in The Republic, Plato likened earthly objects. >uch claim are impressi\e, including such scholars as 

as the li'iangles or hoi'ses we are familial" with, to the 

shadows cast on the wall of a cave liy objects lliat pass by 

the enU'anee. I^ike people within the cave, bound so that 

they face the wall, we see only the shadows, the im[)erfecL 

represcnlatluns, of reality. Likewise, the reality — the 

James Larson (1971) and Frans Stafleu (1971). Yet 
a close examination of all Mayr's sources reveals that 
instead of a literature of accumulating evidence, all 
derive from a single source, an artitde by Arthur J. 

ESSENCK— ol the true equilateral triangle is only imper- (^^^j^^ '^^ ^]^^^ Proceedings of the IJnnean Society of 

fectly eaphired by iIh~ triangles we draw or construct, all 
of which are imperfect, and vaiy from the true, essential 

^Mayr does set out the essentialism stor} lai pp. 4—6 and 
16-17 of his 1963 book (using only the term "typological"), 
but not in his 1942 book. 

London (1958). ThcMc the Oxford zoologist maintained 
that Linnaeus thought in terms of Aristotelian 
essences; the backbone of his claim is that "the 
method [Limiaeus] adopted was to classify by the rules 
of Logical Division, whifdi involve tlu; determination 


Annals of the 

Missouri Botanical Garden 

of the essrnco of each enlity" {(]iun, 1958: Jr>2). name is a Diffcrenlui essefilialis {PliiL BoL, 257) 

(lislinirlli^'lmla lliat speeies from all others in ihe same 



Caitfs ronelusions are now woven into t]ie fahric of 

estahlished knowU-dge, rep<^atefl countless times hy ^renus The Character essenlialis [of a species] is 

people wlu) liave never read hjni. Scholars ulio a Differentia (Plul BoL, 258)'' (Cain 1958: 148). 
sul)se([uendy contriltnled fresh research on l.inriaens, These words of Linnaens equipped Cain to argue diat 
ironically including Cain himself (Broherg, 1985; however messy and complicaltMl his system became in 
Stevens *& Cullen, 1990; Cain, 1992, 1993, 1994, practice, fundamentally Linnaeus must have been 
1995; MTdhM'-WiHe, 1999) are perceived, if they are 
read at alb as supplementing Cain's 1958 conclusiotis, 
even though diey paint a very different piclure. 

A lew years ago I undei'Look a careful cxatninalion 

(^n^as(Ml in this sterile scholastic gam(\ 


The game was indeed schohistic. for 

the procedure 
ol formulating definitions /.;er^''c/;//.v el (lifferenliain was 
an exercise latniliar to geneM'ations of scholars in 
of Cain s 1958 article as part of a project concerned medie\al Lmi\(a-sities, based upon the 6th century 
widi why some scientists turn their attention to scholar Hoetlilus's connnentaries oil anil Latin trans- 
qncstions about the [)ast (\\'insor, 2001). My intfMition lalion of the 3rd century (irct^k scholar Poiph\]T's 

was to investigate the plicnomenon ot scientists 

f sci 

introduction to Aristotle (Kretzmann et ab, 1982; 

turning to history, and both Cain and Mayr were in Si)adc, 1994). Porphyry's notorious "\'\ve words" are 

the prime of their scientific careers when they began rendered by Bocthius genus^ species, di [fere alia, 

to write about history in the i950s. My interest was propria, and aceidens. What C'ain i\\{\ not realize was 

Cain's motivation, not Linnaeus's reputation, but I the extent to which leatlie]-s In Linnaeus's day. and 

found mysell amazed by tlie many weaknesses in indeed many of die mcfheval schoolnien, regarded the 
Cain's argunuMit. It would seem diat Cain's conclu- 
sions took hold because they meshed so \scW with two 

whole business as a taxonomy of words, not things 
(Arnauld & Nicole, 1662). (What Aristotle himstdf 

other semi-independent and sinnihaneous lines of would have diought of it [Balnie, 1980, 1987: 73; 
thought. One was Mayr's association of the mor[jho- CottheJf, 1985J is quite another matt(M-.) If the task is 

logic-al concept of species widi typology, wincli to defim^ the word ''horse,'" a schoolbov learned not t 
included tracing ty|>ology back to F^lato's cave (Mayr UKaition the features peculiai" to hi^ 


ns own mare 

et ab, 1953: 15; Mayr, 1976: 256-257). Anotluu- RosaliiuL sudi as her location and color, anil not to 

strand flowed from David Hidl's 1965 article 'The compose a tedious list of all those f(\ilures, such as 

effect of es.^(Mitialism on taxonomy — two thousand being four-legged and having a mane and tail, that she 
years of stasis." The esscjilialism story known today 

consists ol elcmenis from each strand, which were ap[)roacli is simply to stale the gnjup name ("eiiuine") 

twisted tightly togi;tlier in 1968 when Mayj- (le(;ided [)his the features distinguishing horses from others 
that die concept of species he called ^'typological 

shares widi asses and zebras; the frugal and prop(n- 

(il this group. It was widely understood that thi; 

thinking" could be equati;d with the concej)t of elementary exercise arouses llu^ thitru)- question of 

essenlialism he found in HuH. 1 intend to trace tint whether the al)stract "liorse" (the uni\i'rsal), the idea 

elsewhere the distinct histor)()f those three strands. or type of horsiness to wincli Rosalind somehow 

Cam believed hf^ had made a breakthrough in jjelongs, really enjoys existence in some eternal place, 

understanthng Linnaeus when he learned that Arislo- as ITalo said, or has a n\i)i:c llnn'ted existence as the 

telian logic mandated dial deritiilion should proceed active j)()wer within each individual horse, as Aristotle 

by stating tho kind (^''c/;//,s' In Latin) to wTich a species said, or exists only nominally, as a product of our 

belongs (man is an animal) and then stating the own mind, as WilLam of Ockhani said. Philosophers 

diJfereiUia, die features that dislinginsh it from the debated die (jut^stion, but the relevant point here is 

other members of that kind (man is a rational animal). that their debate did not touch the rules of proper 

Linnaeus's rule that every s()eeies name nuist begin definition. Even for a nominalist, it is efficit^it to 

describe an o]>j(T't that resembles other objects ])y 
first staling the set of similar things, and then pointing 

with the name of [\n 

^enns to which it belongs was 

what had lirsl made Cain suspicious, and then die 

telltale w^orils defmiiio, dijjerenfla. and essenlialis to the f(Vilures b\ ;vhich this one differs. 

seemed to confirm il. Indeed the case seemed bc}ond 
doubt when Cain found a series of incriminating 

pronouncements in Linnaeus's Philnsophia Botanica, also dt^dared "llie concept of a s|)ecies consists of an 
which he rendered as 'The Esscfilial Character of 

The supposedl}" essentialist views Cain qiutted from 
Linnaeus could have been multiplied, for Linnaens 

a genus 

is that 

which gives some characteristic 

essential ieature, by which alont^ it is distinguished 
from all others in the same genus. ... A specific 

peculiar to it, if there is one such, which will instantly definition contains features in which die species 

otluM's in the same differs from those in the same genus. Ihil the specific 
natural order [P////. BoL, 187] The true specific name contains the essential h'atures of the debni- 

serve to distinguish il fi-orn a 

Volume 93, Number 1 


Linnaeus's Biology 


tioii. . . . Therefore ihe specific iiaine is the ess(nitial that "hirer is a genus containing the species "swan," 

definition'' (Linnaeus, 1751: 219-220). (Note tlial for but it is equally hue that "hird" is a species in the 

Linnaeus, (he "name" of the species was nol its two- genus "animal." A person devoted to scholastic 

word sht)rthand form, hut the genus name modilied by principles, wlio decided to set up a system running 
up to a do/en adjectives.) However, il would he a sin 
against a prime principle of historiography (mider- 

standing actions and words in the context of their own 

from Kingdoms containing Classes to Classes contain- 
ing Orders, would be obliged to avoid the logical terms 
genus and species lor the next two ranks, for- each Class 

lime) if we were to assume that Limiaeus was using is a species with respect to its Kingdom, but a genus 

the word essenlialis in ihe same sense as medieval with respect to its Orders. The fact that Linnaeus 

phih)sophers had. Th(? context, as well as his own appropriated these old words and spoiled them by 

definition, shows thai the word only meant "taxonom- attaching them to absolute ranks in his hierarchy 

icall} useful" and nodhng more. What he called the proves his utter disregard (or die "Aristotelian" rules 

"character" of a genus was the list or suite of features 
found to be dependable, and these \m) categorized with 

of logic. 

I am myself no expert on Linnaeus, so 1 was 

three adjectives: faclilius, essentialis, and nalttniles. relieved to find tliat the skepticism to which I was led 
The first was a single feature used in some botanist's by a close reading of Cain had already been 
artificial system: the second was a single feature, or as indf^j)endcntly adopted by Staffan Muller-^llle 
few as jjossible, peculiar enough that it serves to (lW9j through his close reading of Linnaeus. His 
distinguish diis genus from the olh(!r genera in its work, which is not yet as well known as It deserves to 
natural order. The third was the full list of features. be, makes me confident that the tide of opinion on this 
The character essenlialis was dcsiralde because it issue must turn. Yet the process will not ])e easy, for 
enabled the production of a succinct catalog. Nowhere the essentialism story can bicis our reading without our 
did Linnaeus suggest that the "essential"' fealui-es noticing. Consider one significant detail from Mayr's 
were any closer to the inner nature of a plant llian its GrowlJi of Biological Thoughl (1982: 173): "In school 
other features. On the contrar) , he insi>ted that Linnaeus had excelled in logic, and he was evidently 
botanists pursue die characteres naiurales. Liimaeus dee|>ly impressed by the precision of this method." 
(1751: 1 13) wrote, Here we have an instance of history by deduction, for 

Cain's argument certainly does require us to imagine 
that Linnaeus had mastered scholastic logic. Yet Cain 
had no evidence to that effect, so he could only 

If die essential cliaracters of all genera had heeii 
discovered, the recognition of plants wouki turn out lo 
be veiy easy, and many would undta'value the natural 
cliaracters, lo their own loss. But lliey musl undcrsland 
tlial^ vvitlionl regard (or the natural character, no one will 

beguile his readers b} 




every we 


educaled man in and befoie LIrmaeus's time miglit 

tuni ont lo he a sound bolanisL; fur when new genera are liave been given some instruction in the principles of 

classification in general, as laid down by Aristotle. 

disco\cred, the bolanisi \\\\\ al\va)'s l)c In doubt if [he 

neglects the natural character. Anyone ^vho think, that he ^p^-^ ,^^^ ^^^^^^^j^, ^^^^^^^^^ j^^ ^^^^^ ^,^^^,y of Lo-ic. . . " (Cain, 

1958: 145). Notice die ambiguity of the pronoun "he," 
whit.'h cordd easily lie misread as "Linnaeus" though it 

uriderslands bolanv from die esseiUial charat^lcr and 
disregards the natural (jne is therefore decei\ing and 
deceived; for tlie essenlial character carniot iail lo be 
dece|)ti\e in quite a numher of cases. The natural 
character is the fonndalion of the genera of plants, and no 
one has ever made a proper judgt-nuinl about a gtnuis 
without its help; aiul so it is and always will he the 
absolute foundatiuti of the understan(hng ofphuils. 

In erecting these terms, Linnaeus may have had in 
mind the famous exchange between John Ray and 
Joseph Pitlon de Tournefort (Sloan, 1972; McMalion, 
2003), but if so, he was siding with Ray and thuinhing 
his nose at Tournefort, by choosing to define 

projierly refers only to some "well-educated man." 
Leaving aside the rpiibble that Linnaeus was not 
particularly well-educated by 18th century standards, 
Cain's claim is Irue only because of his carefully 
(pialified verb "miglit have been given," An educated 
man might have studied Aristotelian logic, but then 
again, he might not. 

Actuallv there is no evddenee that Linnaeus studied 
logic at all, much less excelled at it, according to 
Muller-^'ille (pers. comm.). Indeed the positive 

essentialis solely by its taxonondc c:onvenience rather assertion of excellence in school is peculiarly at odds 

.11 r ' . 1 ., .- 1 . vvith the slight evidence we do have. Among Mayr's 

som-ees, the one that reports on Linnaeus's schooling. 

than by reference lo a plant's essenlial nature. 

The telhale words that had first cauglit Cain's 
attention, "genus" and "s|)ecies," acTually tcstif} most 
damagingly against his claim that Linnaeus was 

Blunt (1971: 18), says this: 


f losrical di\ision. As 

owing uie rules oi logicai (u\ision. ns every 


medieval schoolboy knew, Roethius's genus and 

species were relative terms. One may correctly say 

In 1724 he passed, though with no great distinction, into 
the Gyninaslnni. Here the curriculutTi was designed to fil 
the needs of line's intenrled for the jiri est hood: the 
emphasis was upon Greek, Ilehi-ew. theology, meta- 


Annals of the 

Missouri Botanical Garden 

pliysics and omlnry — snhjrcts in which he vv;is hllh^ orders were arlificial cleviees, invented to ease 
gillcd and even less itiU-icstrd. Apparently he shone al ideniifieation 

physics and iiuithetnatics 

This is an accurate siiiuinary of Liniiaeus's own 


winch (danns excellence in science 

and makes no mention o( logic (Fries, 1923). The 
erroneous tidbit al)onl his nnl only stndA^inp; lofric 1)[|| 

being deeply ini[)ressed by it may now b(^ hard to 

(M'ase, however, because o( beitig staled so (dearly in 

Mavr's audiurilative book. 

What al.)out Mayr's concern thai in(li\idual differ- 
ences, so cru(dal for Danvinian evolution, would have 
been discounled as mere accidents bv anv follower of 
classic logic? (^ain later showed (1996) (hat the 


¥ * 

ogicians concej)l 

of '^iccident" had considerablv 

faded b} John Ray's time, l)ut Ma>r was surd) coruH't 
ihat taxonomisls wanU^d to find conslafit (diaraelers 
and did llieir l)csl to weed out variable (diaractcrs. 
This was obviously a pra(dical issue, bul wlndher the 

The essentialisiTi slory [hat en":ulfed and incorno- . r i i ,- i ■ i i i . n • 

■^ ^ ^ concepts ot sciiolaslic h)gic puiyecl any role at al! n 


rated Cain's 1958 argument also transformed ih 
AbsenI from Cain's arti(de is the \ery word "ess('n- 

tialism/' which had been used l.)y Karl Popper (^1944: 

18lli century taxonomy, or e\en ui the Iwo pre\ lous 
cenlnries. entn"(d> renianis lo be demonstrati'd. 

Unforlunat(.d\ , [lie esseidialism slor> lias lendcd to 

94d lo expose a lallaclous and dantrt^'ous liabil of i ■ , . • ,i • u i i . r 

^ ^ {hinnien lulerest ni I lie rich anfl compU^x slory ol 

tliongld. Hie lallacy is oik* into which reasonable 
j)eople are prone lo faff, namely, lo believe ihat wc, can 
find out the true nature of something; bv concoctin'>; 
a del itn lion of the word I hat names it. (Actually 

exactly how^ taxonomisls, bolh before and afler 
Danvin, co|)ed wilh tlie real-world idialUaiges of 
comiiarint;!; and ideul if\ iuu orfranisTiis. To h)osen its 

grip, we could begin by recognizing that mallgiiing 

Popper assumed ihat no 20lh century seienlist really Linnaeus disU)rls our nnderstandino- of tl 
belic\ed tins, so he aimed his crilicism at "method- histoiT of svsttanalic-s 
ological essentialisnu" whi(di means acting as though 

one l)elieves it.) Popper's 1945 l)ook The Open Socicly 

and lis Enemies furlher (hweloped the concepl. but 
there is no evidence lliat either Cain or Mayr look 
noliee. David Hulbb 1965 paper, whiidi featured 

le entire 

Lileratuic Cited 

Arnauld, A. .K \\ Nicole. 1662 (1996). bogie ov die Art 



as al 


Poj^per's word and coticepl, was almost cerlamly now 
MaA^r learned of them; Hull mailed him a cop\ ol Ids 
paper, which was the start of Mayr's mentorshi[) of 
Hull. (Mavr verv iiracIousl\ alIo\\ed me lo examine 

Thinking, J. V. Hnroker (transhilor), ('ainhrtdge I'niv, 
Press, Cainhridge. 
lialnie. t). AL 19o(). Vrisloth^'s hioloi^v was not esseiitialisl. 

Areh. Ge.sch. Plnlos. 62: 1-12. 

their correspond(Mice along with his other papers in 

. 198i. Aristotle's use of di\l^ioii and diKei'eniiae. 

Pp. 69-89 in A. Coltlielf >.K- J. G. Lennox (e<hlnrs). 
i''hilosophiea] Issues in Arislotle s Biologv. ('anihridgi^ 
LJniA'. Press, Canihrid^e. 
the Harvard Universily Archives.) Hull recogJiizc^l J3hiiil, W. 1971. The Coitipleat Linnaeus: A Life of Linnaeus. 

lliat there were some problems with Cain's argnin(mt 
(Hull, 1965: 316n, 1967, P)85), l)ul he did not (|uarrel 

with Cain's basic message, lliat Linnaeus wais in the A. Wilson (editor). MIT !>ress, Cambridge. Massaehnsetls. 

business of defining specdes Lke a logician rather Broherg. G. 1985. Ijiine's systenialies and die new nalural 

liistoiy dis(.-o\ erie.^. Pp. l5o-181 /// J. \\ ein.^tock (editor), 
ConteTn]>orar\ l^erspeetives on Linnaeus. I iii\. Pn'ss of 
America. Laidiam, Marvland. 
Cain, A. J. 195M. Lo<rie ami niemorv in Liniia<'us"s svstem of 

la\onom\. Vwk-. Linn. Soe. London 169: 1 J I- 16'L 
. 1992. The Mcllwdiis of Linnaeus. Areh. Nat. Hist. 

Vdving Press, New Yoi'k. 

KoN'th R- TJ9'-J. I iotn(\)slasis. sp(Mdes, and higher laxa. 
Pp. 141 — 185 ill Spe<*ies: New hilerdis(dphiKii\ I'.ssavs. R. 

Llian describing them like a natm-al historian. The 
conneclion bet\veen Popper's concept and Avhat 
bothered Mayr — ''typological ihiiiking" about spe- 
cies — was somewliat loos(^ (Mayr considered Phi to 
rather llian Aristotle ihe eu(an)), bul in general, (Gain's 
assessment of Tiimaeus seemed h) lit into both Hull's 

and Vlayr's view^s ol the historv ol taxonornv. 

When we consider how deeply Linnaeus was 
ste(^[)ed in the literature and traditions of earlv 
modern botanv and zooIo^n . is It e\eu likeb tliat he 
would have fallen into the (allacv of essentialismV We 
need tt) ix'aiize that Po[)per was by no means ihc first 
thinker to warn people against it. The rhetoric o( die 
Seienli(ic Kevtdutiou, iiudnding the widliugs of Hacon, 
Descartes, and Locke, was consistentlv auli-stdiolas- 


tic. It was cdear to ev(M'v slud(Mit of Linnaeus that the 
bu.-^incss of the true botanist was to interrogate nahue: 
after all, he had emphasized lliat his own classes and 

19: 2;LI-25{). 

— - — . 1993. LitmaeusV Orflines JVafiwalcs. Areh. Nal. 
Hist. 20: 1.05-'1]5. 

-. 199L AiiiiH'rus. fii/tira. propi/rlio. silus: Linnaeiis's 

definItor\ attiihules. .Vreh. Nat. Hi>l. 21: 17-36. 


. 1995. LitnuKaisV natural and ailifieial arrantrmenls 

ol |)Iants. Rol. J. l.irm. Soe. 117: ;3— 133. 

. 1996. J. .Iin Ra\ (in "accidents." Areh. .\al. Hisl.23: 


LIlis, B. D. 2002. The Philo.sopli\ of Nature: A Guide to ihe 

iNew Essenlialistn. Me{7ill-(Jneen\s L'niv. Pi'ess, Montreal. 

Fries. T. \L 1923. Linnaeus (alhM'wards Carl von Linne) : 

The Storv ol his Li(e. R. 0. Jackson (editor and Iran^lalor). 
II. F. & G. Wilherh\- London. 

FuluMna. 1). J. 19911. l^xolntionarv Biolof]^\. '\n\ ed. Sinauer. 
Sunderlaiiil. Massaeliusells. 

Volume 93, Number 1 

Linnaeus's Biology 


Gotlliclf, A. 1985. Ntjtf's lowards a stiuly of substance and 
essoiicr in ArisiolU! s J^arls of AnltiiaLs ii— iv. Pp. 25-54 in 

A. Golllielf (t-ditur), Aristotle on Nature and l.i\ ing Things. 

Vlathesis Puhlifalirtns. Pittshui'tr. 
Greene, E. L. 1909. IJnnaeusas an e\{>lutionist. Proe. Wash. 

Acad. Sci. 11: 1 7-26. 
Hull, D. 1965. The t^deet of (;ssentlalisin on laxononn — two 

, E, G. [.insley & R. P. Using<-i. 1953. Methods and 

Principles of Systematic Zoology. McGraw-Hill, New 


McMahon, S. 2003. John Ray. Joscpli Tournefort and 
essences in the seventeendi Centui'}. Paper deh'xcred at 
July meeting of the International Society for the History^ 
Pliilosophy, and Social Sludies of Biology in \ icnna. 

thousand years of stasis. Brit. J. Plnlos. Sci. 15: 314-326; Muller-Viillc, S. 1999. Botanik und Weltweiter Ilan(l<-h Znr 

16: 1-8. 

— ■ 1967. Certainty and circularity in cyolutionary 

J ^ J 

taxonomy. Evolution 21: 17'^l-lo9. 

-. 1985. Pinne as an Aristolchan. Pp. 37-54 in Jolni 

\^V'i 11 stock (editor), Contemporaiy PerspfH'ti\'es on Lin- 
naeus. Univ. Press ol America, Lanham, Mai"\hniil. 

Koerner, L. 1999. Pintiaeus: Nature and Nation. Harvard 
Univ. Press, Canihridge, Massachusetts. 

Kret/mann, N., A. Kenny & J, Piuhorg (editors). 1982. The 
CainliridiTf? Plistorv of Later Medieval Philosophv from dir 
Rediscoven' ol Aristotle to th(^ Disintt^^^ralion o( Scholas- 
ticisni 1100-1600. Cambridge Lni\. Press, Cambridge. 

Larson. J. 1971. Rcas(jn and Expcricnt;e. Uidv. of CaHfornia 
Press, Bcrkele} . 

Linnaeus, C. 1751 (2003). Pluh)sopliia Rotanica, S. Freer 
(translator). Oxford Univ. Press, Oxford. 

: 1753. Species Plan tarn m, 1st. ed. Impcnsis 

Laurcntii Salvil, SttK'kliolm. 
Mayr, E. 1942. Syslematics and the Origin of Species. 

Colnml)ia Univ. Press. New York. 
. 1959. Darwin and the <noIutionarv dicoiT in 

bioh)gv. Pp. 1—10 III B(Hty .L Meggers (editor), l^volulion 
and Anthropolog) : A Centennial Af)pra]sal. Anthropolog- 
ical Society of W^ashinMon. VV ashinfrton. D.C. 
. 1963. Animal Species and l^\olulion. Relknai) Press 

of Harvard Univ. Press, Cambridge, Massachusetts. 

. 1968. Theory of biological classification. Nalur<' 

220: 545-548. 

. P)7f>. Evolution and tlie Dixersitv of Lilo: Selected 

Essays. Belknap Press of IIar\ard Lniv. Press. Cambridge, 

Begruiiduug eines NaLurliclien Systems der Pllanzen 

duroli Carl \()n Liiiuo (170/— 78). V^n'lag fiir W^issenschaft 

und Bildung, Berlin. 
Popper, K. 1944. Thf^ pov(Mly of historieism I. Economica 11: 

. 1945. The OpfMi Society and Its Enemies. G. 

Routlcdgo, London. 
Ramsbollom, J. 1938. Linnaeus and die spet;i(^s concej)!. 

Proc. Linn. Soc. London 150: 193-219. 
Sloan, PhilHp R. 1972. John Locke, John Ra)', and the 

problem ol the natural system. J. Hist. Biol. 5: 1-53. 

Spad(^ P. V, (editor). 1994. Five Texts on the Medieval 
Problem of Universals: Porj>hyry, Borlhius, Abelard. Duns 
Scotu^. Ockham. Hackett Pubbshnig. Indianapolis. 

Stalleu, F. A. 1971. Linnaeus and tlie Linnacans. Oo^tlloek, 

Stevens, P. F. & S. P. CuUeii. 1990. Linnaeus, the cortex- 
medulla iheoTy, and ihe key to his nnderstanrling of plant 
form and natural relatitmship. J. Arnold Arbor. 71: 


Whewell, W. 1847 (1967). The Philosophy of the induc- 
tive Sciences Founded upon Their History, 2nd ed. 
Facsimile reprint, Johnson Reprint Corporation, New 

Winsor, M. l\ 1991. Reading the Shape of Nature: 
Comparative Zoology al the Agassiz Museiun. Univ. of 
Chicago Press, Ciiicago. 

. 2001. Cain on Linnaeus: The scientist-historian as 

. 1982. Tlic Growth of Bitdogicai Thonglil. Belknap 

Press of Harvard Univ. Press, Cambridge. Massachnsells. 

unanalysed entity. Stud. Hist. Phil. Bitd. & Biome*]. Sci. 

32: 239-254. 

. 2003. Non-essentialist methods in pi'e-Dar\vinian 

taxonomy. Bio. & Philos. 18: 387-400. 


David B. Wake 

2. 3 


I hat an^ linked liv a[i[)ai"ciil cliiial varialioii in inh^'grarlr zones, 

Mow many species one recognizes willnn a gi\en taxnn remains a tliffuaill question. espt^cialK \\ hen nior])holog\' is 
rehiti\elv stable or when clinal \"ariati(>n is present, thus eoniphcninig iliagnf>sis. T accept the general lineage concept of 
species, aiul my goal is to recognize liistoricalK clislinct evolulionary Hneagt^s that are likely lo remain (listin(T. Here T analyze 
lliis task with respccl lo |)atlerns of specit;s ioinialioH in two genera ol ph'thodontid salamaiulcrs in Caliioi'nia. Ensalina Is 
a ring species coni[>l<^\ suri'ounding tlit^ ('enli-al Valley of (>ali(ornia. At [)resenl it is a single spiM'ies with seyen s[]|)speeies 

I tut llna'c are also some naiiTnv Inlirid zones where 
nioi[)hologically and ecologically Jilferenliated forms interact. In ((tnli'ast, Biilrnchoscps, which has much die same 
distribution, has about 20 sj,)tH-ics in Califoinla. most occurring in s\ inpat r\ with Ensdlinu. Di\crgenc-e in tlie two tax a i^ based 
on two fundamcntall) dilleretU [)henomcna, and \('t there are soni*; c(;tnnioii themes. Ada])li\e di\crgcnce in coloration \> the 
dominant theme in KnsaluKi, whereas dinerentiation is largel\ |i<M-cci\f'd al the molecular \c\v\ in Hdtnichoseps. \et both luue 
evolyed in iIk^ same n^gion and have been aficet4'd by man\^ of the same cliinatie and earth historical phenomena. Within liie 
Frusalijui complex, tliffcronl adaplalions ridated lo predator ayoidance have evolved. C<jloratioii has divergetl in <h(ferent 
directions '\n coastal and inland populations, even though genetic interactions contituic to take place. Where coastal 
]K)pnlations ukmH ollu'r coastal popuhilions, ecologically and morphologicall) similai' populatitms iiuM"ge genetically, vxcu if 
\v(dl (hfferentiated in molecular traits. In contrasl, where thi^ ring is cross(Ml and where ecologically and niitrpliologically 
differentiated jutpulations meet, they hybridizi' narrowh' or are sympatric and behave as if lhe\ are species. Within the ring- 
like distribution, i linal patterns of variation occur. The current poK t\ [>ic taxonomy is retaineti, even though it i> problematic, 
because alternati\es are e\en less approjjriatr\ In contra^^t. where gciuTlcallv differentiated ])o[)ulation.^ of Batnit lioscjis meet 
they tspically do nut merg(\ Instead, they replace one anothei" spatiall), in j:)art because' they are so similar ecologicall) . 
Apparently the periods ol isolation were sndicientl}' long that even in the al>sen(*e of nda[)li\'e divergence there has hccn 

ifferciitialion in allozvmes and mtl3NA in rtdation lo the 

divergence oi isolating mechanisms. Analysis of pallcrns of genetic i 

geological histoiy of (^aldoinia is used lo generate biogeographic sciaunios lo help explain the contrast between Batradiost'i/s 

and Ensdfina. 

Key irords: Bdlrachosrps. California paleogeograjihv. Ensafina, historical l)iogeogra])hy, ph\ !og(V)graph}', salamanders. 
species formation. 

Every generalioii of biolugisls is tlestiiu.'d Lo deal salainaiiders is based on such erileria. W Ikmi 
with species problems, somelinies repeatedly, or, in inobM'iilar methods became accessible to systemalists, 

my ease, cotiliiuiously llifouglioul my career. I 

roimblv l\o years a^^u, many sLiri)rises residled. Kav 
described my first new species in 1962, based on Yatiev. tlu^ fiist to use sueii nifMhods m m\ lab, found 
a single specimen from Colombia lliat had been that alIo/\mes nnco\ere(l diflerent patLenis iban did 

moi'pbolog) III llie Slender Salanianrlers [Bafnichosrits 

collected in tl 

le uineleenlh eentiny and assigned to 

a species thai was thought, mistakenly, lo range IJoiiaparte, 1839) of California (Yanev, 1978). Se\eral 

nominal species were spet:ies complexes, and a mnn- 

llnongliout Middle America and into South America 

(Rrame & Wake, 1*>()2). That species has so far stood l)er of imdescrlbed species were identified (Yanev, 

1978). James Hanken. ahso in mv lab. made similar 


le test of time, although even today it is known from 

fewer than 10 specimens. The decision to describe the obser\ali()ns on tropical salamanders of the genus 
species was based solely on anatoni) and color ThoriiLs C(tpe, 1869 (Ilanken, 1980). Ricdiard Highton 
pattern. The vast majority of all known species of w^as among the first svstt^matists to use molecular 

' Many individuals have collaborated with tnc in the research sumrnari/<'d here, and 1 thank especially C l^i'own. M. tV<do\\', 
H. Hansen, M Jockusch, S. Kuchta. C. Morilz, T. Pa])(Mifuss, D. Parks, C. Schneidei', \. Slaub, M. Wake, T. \\'ake. and K, 
Yane\. C. Brown ])erniitted nie to use man) of his excellent photograph> i)f Ensaliiia. The figures are by Kanai Klitz. I 
appreciate the helpful comments of Shawn Knchla and two anonymous re\ lewr^rs, hinaiUMa] su|)j)ort for mv research from NSF, 
the Gompertz Professorshii) of m\- uni\'ersity. and the Museum of \ ericbrate /oolocv is L!:ratefull\ a<-kriowled":ed. 

^ Dc[)artnient of Inlegrattve Riologv and Museum of \'ert(d)ra!e Zoolog\ . l^niversity of ('.nlifnrnia. Berkele\ . (California 

94720-3160, U.S.A. wakclab@uclink.berkclc).cdu. 

* 1 dedicate this paper to ii. C. Stebbins, who remains an enthusiast for Ensalina, on the occasi(jn of his 91st birthda\ , and I 
the memory of Ardcn II. Hrame Ir. II (lU^Vl— 200 Ij, wlu) first inlroducnl me to Biitrachosrps and its diversity. 


Ann. MissoiRi Bot. Cajid. 93: 8-23. Puritsiied on 31 Ma^ 2006. 

Volume 93, Number 1 


Species Formation in Salamanders 


methods in comprehensive geographic sami)1ing; soon 



le uncoverc 

d level 

eveis o 

hat species are recognized. The critically Iniptjrtanl 
f differentiation that were point with respect to the general concept is that tliere 
previously unimaginable (e.g., Highton. 1989). Before are no necessary attril.jutes of species; rather, ihere are 
the main impact of the new molecular systematics different lines of evidence that can he used concern- 
revolution, the first modern complete catalog of ing separation of lineages and these are all contingent. 
amphihians reported 356 salamander species (Frost, The pragmatic matter of delimiting species remains, 
1985). The numhcr of salamanders has increased however, and man) methods have been proposed to 
since by 56% (the most recent count is 556, deal with the issue. All are problematic (reviewed by 
AmpliibiaWeb, 2006). These an; surprising increases Sites & Marshall, 2004). Furthermore, even adopting 
for a group of relatively well-known terrestrial die concept framed by de Queiroz does not mean that 
vertebrates, especially given that niany of the new 

different taxonomists will reach the same conclusions 
species reflect new discoveries. Mowever. the new because criteria can be interpreted in different ways. I 
descriptions also highlight a modern species problem suspect that de Queiroz (based on de Queiroz, 2005) 
that is not unique to salamanders, but common to most would recognize more species than I would in most 
taxa — how to translate molecular finthngs into instances, because of his emphasis on detection of 


At the same time as new laboratory methodologies 
were drawing attention to species prohh-ms, new- 

initial spUts. 

Pattkhn and Proci-:ss in SrECiES Fokmation 

phylogenetic methods were 


nig a major nnpact. in 

t. 1 

particular, methods ranging from mainly phenetic 
n-ical taxonomv to cladistics were causing 


Classifications of modes of species formation may 
be pattern-lxised or process-based. By pattern 1 refer 

systematists to retliink species concepts and criteria in particular to geographic units inferred to be 

(e.g., Cracraft, 1989, 1997; Mayden, 1997). As genetic itidependently evol\-ing lineage segments, i.e., spe- 

analyses became ever more sophisticated, renewed cies. Criteria vary greatly, from some relative measure 

focus on species was one result (e.g., Templeton, of degree of divergen<^e to tree-based approaches. The 

1989; Coyne & Orr, 2004; Hey, 2001). simplest way to explain such patterns is vicariance 

Given the sheer volume of recent publication on plus something else, such as differential selection or 

species concepts and on the species problem in even haphazard changes in gene frequencies. By 

general, it is a bit surprising that de Queiroz (1998, process I refer specifically to adaptive processes that 

2000, 2005) concluded that no fundamental change in are critically important to the establishment of 

our species concept lias taken place and that such independent lineages. Although an enormous amount 

a change is unnecessar)\ I agree with this perspective. of literature deals with species formation, 1 locus here 

There are indeed many ongoing debates about on adaptive divergence and nonadaptive radiation, 

species, but these are fundamentally about criteria These arc alternative ways that lineages diversify. The 

and the debatt- is mainly joined by proponents of main problem that has been id(MUified witli adaptive 
different kinds of data or more explicit methodologies 
than used in the past. 

divergence is the estabbshment of genetic isolation 
between die adaptively diverging populations when 

Here I examine patterns of species formation in they are not allopatric. The main problem with 
Californian salamanders that display contrasting nonadaptive radiation is the historic one of de- 
patterns. My goal is to highlight the connection of termining the status of geographically isolated but 

pattern and process in the formation of spec-ies. 1 am 

phylogenetically ndated parts of lineages, the classi- 

especially interested in comparisons of tree-based and cal problerTi with allopatry. 

character-based methods of delimiting species and 

what it is that we have delimited using these methods. AdaptjvI:: Duercenck 

In addition, I ex])l()rc whether species recognition and 
delimitation is an exercise in recovering historv or in 
predicting the likely course of further evolution. 

Papers by Cush (e.g.. Bush, 1969) and a book by 
Endler (1977) are the starting points for my own 

has been developed by Mayden (1997) and de Queiroz 
(1998, 2005). Species are historical lineages of 

I accept the general lineage concept of species ihat interest in adaptive divergence (as opposed to the 

historical allopatry arguments) as a factor in species 
formation. Bush emphasized adaptive divergence in 
metapopulations, or, more precisely, they are seg- sympatry. Endler was more interested in geographic 
ments of metapopulation lineages; all other considera- variation, in particular clines in characters or gene 
tions are secondarv to this primary prineij)le. In any frequencies, and appearance of steps in clines, which 
given instance, one might rely on any of a number of might be preludes to species formation; his emphasis 
secondaiy species concepts as criteria to delineate was parapatiw or alloparapatry. 


Annals of the 

Missouri Botanical Garden 

My studies ol cHlaplivc (llvergrncc \\i\\c [ocused on j)ir!a Wood, 1940, A\ e. plalcfisis, E. e. Xdnllioplica 
the plcUiodoulid salatnander Ensalina Cray, 1850, Slehhiiis. 1949; Fi<i. 1). He envisioned an ancesloi 
v\liicli i!is[)lays goograpliieal differentialittti interpreted 
as cllnal ddlerenliation and adapti\e divergence on the 
way to species forinatinn (SLel)hins, 1949); it remains western California. This form has a somewhat xiim 

lui\ing the traits o\ pictti. restricted no\\ to the ancient 
loi-esls of soLithwesLern Oregon and extreme futrlli- 

prohl(M7iatie whelhc!- subsets of the 

ineage have 

gated color pattern, and in it Stehbins envisioned tlie 

achieved independence and how many species vvairant pol<Mitial of all of die pallerns found elsewhere. Ivicli 

4 1 

recognition. Efisatina is 

a ring species com 

pi ex, 

a taxonomicall) (4ialh 

■ngmg grou[) 

snl)S[)(M-ies was diagnosed on the basis ol' its color 
of populations pattern and :^ome subtle morphological dilferences, 
s|)read from British Coluinbia to iJaja California. although oregonensis was something of a dcfauh and 
generally west (tf the Cascade-Sierra Nevada mountain had highly varialjle color pattciirs. From a pichi-Wke 

ancesloi' Slebbiirs postulated southward rTiigrations 

aecompani<Nl by divergcnl ada[)latloii. In the Sierra 
They display direcl development (Ictatolrophy) in Nevada the forms Ijecame reslricted to motilaiu^ annis, 

which embryos form inside the egg capsules and hatch usually with closed canopy forests, and llu^se 

system, lliese arc terrestrial salamanders that never 

1 tl 

enter water, and ttiey never gather in assem1)lages. 


as miniatures n\ th(^ adult. Ensatina is relatively long- thought to show [)rogrc;:,sIve slage.> in the develo|>nicnL 

li\('d (ca. 8 years), sedentary, philopatiie, and shows of (h^rnjitive coloration, bom intergrades in the far 

bttle dispersal (Stebbins. 19S4; Staub c\ ab, 1995). north to sj)otted red and brown /j/r//en.s7.s\ to more vivid 

Prior to Stebbii]> (1919) lour species were recognized. )ellow and black rrocraler in the Tehachapi Moun- 

1 althouirl 

^ 4 

and a]tiu)ugn some orignially luid been d(^scril)ed as 

tains, biially culminating in the boldly blotched 


)ers o 


le genus Elclhodou, Ensdluia long has khnihcn in the far honlh 

Fig. 1). Along the coast 

the generalized oregoficnsis is variable within and 

been recognized as monophyletie (e.g., Dunn. 1926). 
Three of the species, Ensdtina croccdtcr (Cope, 1868), among popuhitions in coloration, displaying geucjallv 
E. kldiiben Dunn. 1929, and E. plalciisis (Jimenez de cryptic coloration, but not disruptive in pattern. As 
la Espada. 1875). w(^re boldly marktul (sj^otted or 





po[)nlatM)ns l>ecame increasingl) associated with nioi-e 
open habitats, a mimicry relationship develo])ed wllli 
Inner monlane areas from MoiinL Lassen, the dangerously poisonous lunvts {Tunclia (h'ay, 

>lotehed) salamanders associated w ith forested ix^gions 

California, southward to San Diego (bounty and 

1850). Mliuicry Is most highly developed in xanlhup- 
northern Baja Caliloinia. A more w i(l(^spi-catl s[)eeies, ilea, iiiainl} found in the inner coast ranges east of San 
E. eschscholtzii Cray, 1850. was mon^ uniformly Francisco Bay (Kuclila, 2005). 'Daese aposematically 

\ i\ Id \'eMow an( 




colored, lacking s|)ots or blotches, and was distributed colored atiimals disiilav 

along tlie coast of (^ahloinia and Inland as well, to the colorati.)n that conti'asls sliarply with the dlsruptl\(^ 

Cascade Mountains in Oregon, Washingloiu and Brilisli 
Columbia. This Jorin js associated with woodlands in 

patterns of the blotched inland forms. A(la])live 
diveigenee was aecelerati^] as a result of these 



♦ 1 

condition. W hen I he contrasting e.sy7/AY77o//j// 

n 1 

the north, bul in central and south(M-n (California it altf^-rnative adaptations, each different from the 
frequently occurs in more open habitats such as coastal 

sage scrub and clia[»aiTal. and hlnubcri contact each other at the southern (^xlciit 

The conclusions of Steblhiis's (19 19) groundbrcak- of their ranges, they look and acl like diffei-eiit >pecies 

ing study were re\(jlntionary. lie [>ostulated thai the (Fig. 1). although they often h\bridi7e. Critical to 

four, then-recognized, species were part of a single Stcbbiii>\s interpnMation was a "transvalley leak," 

a relatively recent invasion o( I he coastal xonlhopdra 

expanded its range souihward, adaplively diverging into the foothills of the Sierra Ne\ada, where it came 

in different directions in the coastal and inland into contact \\\{\\ philaids and the two hvl)ridized. The 

lineage thai had originated in die noitli and had 

niountalus. Stebbins 

recognized seven subs 



] bv tl 

ring was ToiiueU ny tUe nitergraoing j)0[)i 

ad I 


ons o 


(Ensdlina esrhschn/fzii rschschohzii. E. c. croccater, piria, oregonensis. i\\u\ plutcnsis at the northern end of 
E. e. kluuheri,, E. e. oregonensis (Ch'ard. D-)56), E. e. the Sacramento \'allev. 

Fijiiirc 1. 

E/isalliKi \\\i\\ are found in (^al ifntiiia (all except the hrst tiinilioned ])ti(tt()gnip[i('fl in llial state). Oiversc co\uv 
pallerns ol tlie sul)s])eeics of Knsalina. Ctoekuisc from uppei- tril: EiisinLiia eselisehollzii (jngo/iensis from KiuinL> Co.. 
Washniglon (photo Ij) 1). H. \\ ake); E. e, orcgofwnsts fnnti S(^nunia Co. (C. W. Hrown): intergrade l)el\\e(-n H. e. oregnnensis and 
E. e. j)l(ilensis fnmi Stiasia (.^o. (C. ■W\ thrown): northern E. e. plalcusis Iroiii Cahneras Co. (C. W. Brown); .-oiilhei-n A", r. 
platcnsls [lom Talarc Co. (D. B. W ake); E, e. eroeealer Uum Kern Co. (C. W. Bn)Uih: E. e. klauheri from San Diego Co. (C. W . 
Biowa): E. e. csehsrhohzii fr.mi Sati Diego Co. (C. W . Hi-own); at hotlom. a presum]»li\e F, tixhrid t)eh\L'en /::. e. klduhrrt and E. 
i\ esehseltohzii i'roiu San Diego Co. (C. \\\ Bnn\n): a h\hild haekero.s^ hrhveeii E. c. xanlhoplica and E. e, platensts fmm 
(Calaveras Co. (C. \\'. Brown); /':. e. xaulhrfphra in. in Sonoma Co. (C. W. Brown); E. c. xanlhopliea from Calaveras Co. (C. W. 
Br(nvn); E. e. pida from Del Norte Co. (C. W. liiowii). 

Volume 93, Number 1 


Species Formation in Salamanders 


Ensatina complex 

in California 

klauberi x eschscholtzii 


Annals of the 

Missouri Botanical Garden 

Siil>sef]Lirnt research lent some sii|)i)f)rt to the (1049) luul ]i\])c\t^d picia, picia/oregonca.sLs intergrades, 

liypollicsis of Stebbiiis, l)ut a(l(l(Ml complexity. Al- oregoni'iisis, and oregonensis/plalciisis intergrades. A 

lliongli some hybridization occnrs in sonlhern Cali- second chisler included only pUilcusis from the 

fornia, ihcre is much more in the Sien'a Nevada northern and central Sierra Nevada, and the final 

(Brown, 1974). At the southern-mosl [)()int of contact clnstei- inchided />/a/en.s7'.s- from the soutluM^n Sierra 

in San Diego County, no cuiTcnt or past li\ bridization Nevada as well as croccalcr and kltiubcrL Noilhcrn 

has been detected (Wake et ah. 1986). Many plaU'iisls was closer to populations in the northern 

evolnhonists [kicked up on this (^xample as one cluster than to southern /;/f;/e/M'/.v, but a [)oi)ulation from 

illustrating stages in a gradual process of species Wa^er IJidge, west of Yoseinlte National Park, was 

lormalion (hiven by adaj)ti\'e di\'ergence. Ensatina inlermediate l)elweeii the two gronj)S. 
became a textbook example. Dob/hansky (1958) 


I tl 

extended the liypotlu^sis by envisioning gene flow 

e nucstigated these patterns in more tletail using 

tlie mitochondiia 



cytocnrome n gene (Morit/ et ab, 

dn-oughout the ring relarding species h)rmation and 1992). As expectt'd, by 

i i 

examnung distributions of 

lea(nng to Uie persistence of hybridi/alion in the haploly[)c chnh'S, sharp borders ])etween groups of 

center of the ring and in the soulli. Slebbins (1949) p()j)ulatlons wen^ found, notald) between noillicrn and 

had not discussed gene flow; he was [hinking not of soudiern plalcnsis. We also found a sharp break 

a continuous process but ntie in whicli there was between nordiern platcnsis and orcgo/irnsis/jilatcusis 

fragmentation, isolation, and (hvergence, and then intermiuh^s. The scale still seeiiu'd loo coarse, and 

recontaet. In other words, hir, view had elements of snl)s(Min(Mitly we expanded ihe sami)b*ng to saturate 

])oth vicariance and ada[)tive divergence. It was his the Califoi'iiia range of the genus, including nearly 

biogeographical scenario that led him to consider It dOO samples (Knehta et ah, in prep.). Rased on several 
a ring s|)ecies (Stebbins, pers. comm.). 

\\ hen genetic methods became a\'aihibk' 1 initiated 

diderent analvses w^e found it convenient to reco^rnize 
1 1 clusters ol haplotypes (Fig. 2) bas(;d on j)atlerns of 

studies ol Ensatina, expecting it lo l)e a complex of phylogenetie relationships anrl geographic distribn- 
several to many species. Indeed, \\r fomid (^xtensive tion. Most of these are well su|>[)()rted statistically, but 
genetic dilfenmtiation in abozymcs (Wake & Yanev, some (e.g.. B) appear to be parai)li\letic and others 


ciuTemiv recoiin 


1986), but thought our sampling density loo coarse to (e.g.. F.) intduch^ members of two 

detect si)ecies borders (for a contrar) view, see subspi'cics. The northern (postulated ancestral foirns) 
Ilighton, 1998). Difterenliati 
sonlh end of the distribution thii 

on was greater al the 


m m ine rciiion across 

j)ir!(i and orcgonensis comprise six of these groups. 
Again, northern and southern plnfcnsis are differen- 
tiated, vvilli sonlhern po[)ulations clnslering lighlly 

the upper end of Sacramento Valley, and xunllioptica 

■dwd pldlcnsis were less differeniialed from each other wilh rroccaler (Fig. 2); there are three cladcs in this 

than were eschschollzii and kUntheru as would be cluster, each with strong support. 

ptcdicted by die Slebbins model. Many of the genetic 


n>re ( 

lelailed study ol the Siei-ra Nevada contact 

distances between adjacent sam])les were relatively /one focused on the hybrid zone between /y/a/c/i.s/ls and 

high, and we suspected tliat finer sampling was xanfljopfira (Wake et al, 1989). This transition is 

necessary to find either species borders or the gradual sharp, Ituolving 8 fixed or nearly fixed allozvmic 

genetic lransiti(jns as expected under an isolation bv maikeis that change in onlv a few hundred meters, 

distance scenario. We conld readil\ reject Dobzhan- ^fhe hvbrid zones have been stable for about 40 vears 

sky's hypothesis of ongoing g(Mie flow llu-oughout the (first recorded by Brown, 1974), and may lu 

1 \ e 

complex. In general, the coastal foitns (dustered with naicowed o\er a 2n-year period (Alexandrino et ah, 
the widespread orcgonensis, and the blotched and ZOOr^). The distinction between the brightly colored, 

spotted forms in the south clusttMXHl together in 

lowland .vdnllntpllcu and the ciy[ttie, upland pintcnsis 
phcuctic analyses of the alhtzyme data. Mowever, the occurs in an ecolone between lower elevation open 

l)lotch(Ml platcnsis was highly differeniialed. 



oak-pine h)resl and chaparral and hii^hci <devation 

northern ])o[)ulations (dustering with the unblotched closed canopv mixed conifer forest. Few V^ hvbrids 

coastal forms and the single sonlhern population are found, l)ut there are manv backcrosscs. r>ecause 

analyzed clustering with croccalcr and klaiihcri. parental types are s\ atopic, they would lu^ considered 

In order to provide lurther resolution we expanderl distinct species by most taxoiiomi-ls were It net for the 

research to many populations extending {\\m\ picta in pattern in the remainder of the complex. The 

iiorlhwesl<a-u California io klauhcri in the sctulh (Jack- distribiilion of xanfJioptica extends for about 100 km 

man & Wake, 1994). The pojailalions resolved into in ihe foothills of the Sierra Nevada. Tlicst^ po|)ula- 

which patterns ol tiorrs are lillle thfferentiated bom eoaslal populations 

three general clusters, within 

isolation by distance were (h^tecled (.lackman & Wake 

o[ xa/illiopfica in allozymes and tntDNA, as well as 

1994). A northern cluster included what Stebbins coloration. FIvbridization luis only betai sliidied in 

Volume 93, Number 1 


Species Formation in Salamanders 


oregonensis A 
picta B 
picta B 
oregonensis D 
platensis G ^ north 

oregonensis F 
platensis p 

croceater ^ 
klauberi K 

oregonensis C 

xanthoptica I 

xanth optica H 

eschsctioltzii J 



200 km 

Figure 2. EnsaUna in Calilbrnia. Left. Distribution of h^iplotypc clades idontifioil using ihe uiiux'honclrial DNA gene 
cytocliromr b. Right. Pliylograni of Bayosian analysis (if cytoclir'ome sequences for nearly 400 samples of Ensniina from 
throughout llie range of the genus. This is a preliminary analysis from a study in progress (Kuchta el al., in prep.). Clades with 
posterior probability of support at levels from 95%-100% are shown with thick lines. Some of the groups are not clearly 
clades, but \\\i'.) consist of relati\ely closely allied haplotypes that are geograjihically contiguous. The terminal groups are 
labeled and keyed to die map. 

detail in the north (Alcxandrino et al.. 2005), but the allozyme traiisition first is detected, and 1 believe 

hybrid zones are also known to occur betw^een southern that the variation may be a consequence of the merger 

platensis and xanthoptica. In contrast, wdiere norlhcrn of two genetically (bfferentiated populations, 

and southern platensis interact there is no evident Jackman and Wake (1991) presented a possible 

difference in coloration nr habitat preference. 1'he scenario to account for the historical biogeography of 

genetic distance (Nei, 1972) between "pure'' norlliern Ensatina in the Sierra Nevada. They envisioned an 

early southward migration and dilferejihation of 

and southern platensis is 0.26-0.30, ^^'\\h major 
frequency differences in three loci. The genetic spotted and blotcfied salamanders, then geographic 
transition as determined from allozymes takes place isolation as a result of a gap in the distribution that 
over about 300 km, but a mcijor transition in haplolypes de\ eloped midway along the Sierra Nevada. Sub- 
takes place Jiear the southern end of ibis region, about sequently the northern Sierra Nevada w^as occupied by 
75 km south of the major zone of adozymic transition precursors of novihtivn platensis, which in turn ])ecame 
(Wake & Schneider, 1998). Extraordinaiy variation in isolated from oregonensis by repeated volcanism and 
color pattern is found in Yoseniite Valley. This is wliere glaciation in the region of present-day Mt. Lassen, in 


Annals of the 

Missouri Botanical Garden 

norllteasteni Ctilil(>iiii;i. INorllieni and soiillicrti j)la- the sonlh is conx^'t, but the int(M"f^ra(!ati()i» in the norlh 

lacialloii may he s(.:c;oii(lary I'ather lluui pritnar), and sxnipaljy 

Lciisis remained 

se [ ) a ra I ei h 1 1 rubal.) I y 1 ) y ^ 

ronefMitrated in the i]o(']i valleys of the central Siej'ra Avith no hvl)ridi7.ation is fnund in onlv one of fonr 

Nevada assoeiated widi ihe nresent-dav Tuolomn(\ hv])rid zones in the soulh. While svm|)atr\" willi no 

Mtaced, and San Joatinni n\er eanvons. nntil late Inlaidization is found at one sit(^ in the extreme soutli. 

Pleistocene, when the two groups met and merged hyhridizali(tn is documentcnl lor three otlier klaubcri 

gent^lically. A S(decli\c: sweep is resjjousihle for lapid isolates (Wake et ah, 1986). 

The situation on the coast is far from simple. There 

norlliward movenuMit ol the strongly adaptive hlolclunl 

cuh)r pattern of sonlhcun philcnsis (Wake & Stdmei- are two separate haplolvpe groups associated Avidi 

{\{'\\ 1998), This pa!t(M-n is postulated io have s])read to flislineti\"(^ alloz\ mie-based ehist(M's of populations 

the northern end o( the range of tlie northern i)J(ilc!isis within xanlJ\i)j)lic(i, one on the soulhern San Francisco 

haplolvpe group, in the Mt. Lassen area. Slehhins Peninsnhi and the other wideK dislrihuted to the north 
(1949) thought that populations in rujilheaslern 
California were Intergrades between oregofieiisis and 

and east of San Francisco Ba\. incluchng in the 

Sierra n foothills. There are complex interact utns 
northern /;/c/^e/?.v/.v. An all(M-native interpretation is that where oregofieiisis (with two hai)lotyjie groups in the 
strongly marked (but not blotched) salamanders in this region) meets xanllioplica north and south of San 
area thai differ from northern philrnsis in bftth Francisco Ray (Fig. 2; Wake, 19^)7). Furthermore, 
allo/ymes and mtDNA might b(^ an indication that eschschollzu is more differentiated (with respect lo 
soulhern j)hi(e!is!s color alleles have only recently haplotvpes) than MT)nI(l lia\t' been anticipated froni 

the earh alloz\nie study, with distmcti\c northern ant! 

southern g(M)graphic segments thai (orm only a wi^akly 

reached this area (e.g., Fig. 1), where they are 
introgressing into orcgonensis. 

The combination of allozymie and haplot)pe in- snp|)orled possible elade. 

formation led Ilightoti (1998) to conclude thai there is 

Tht;se considerations led me to propose an 
a broad hybrid zone se[)arating northern and southern historical biogeographic hypothesis for the comph^x, 
j)lati.'i\sis. which he coirsidered to be separate (but approximately 5 million years before present, which 
unnamed) species, lie was silent with resp(H*l to postulates a widely distributed orcgoneusislpUitcusis 

1 in- precursor in tlie north, an isolated [jrccursor of 

coloration. Howe\ ei 

, in m\ \ lew . luc zone o 

. ii 


teracllon is far too broad (at least 7S km) lo be northern pht tenuis in the northern Sierran 

considered a hybrid zone. 1 consider a hybrid zone lo and a precursor of southern philaisis/croccater/kldu- 

[)c a site either where two ddferent parental h)rms co- heri in the soullu'ru Sierran region (Wake, 1997). The 

occur and form hybrid individuals, or where two Central Valh^y of California was at this lime an inland 

thilerent parental h^rms are sejjarated by a distance extensi(»n of the Pacific Ocean, and the precursors of 

equivalent to a few. on the order of tens, of home xaruliopfica/rschschollzii may have originated on an 

ranges, ^vith the intervening area occupied by hybrids archipelago (cf. Biitrachoseps scenario, below). How 

and perhaps se\eral gen<-rati()!ial backcrosses. I ha\'e die\ got to lh(^ archi])elago is uncertain, but because 

argued elsewhere (\\ ake, 1997) that any of s(^veral 

■ taxouomic change are probicfnat ic, in the soulh. Paiks (2000) postulated that an early 
and have relaiiK'd the taxonomy of Stebl)ins (1919) 

until compelling e\ idtmce of species borders aroinid 

(as i-ontrastLul with across) the ring-like distribution of preciu'sors of xmuliopdra/eschsclnillzii. SubsequenI 

hnsahnd is found. W hen morphologically and eco- orogenic as well as plate movenicnls led to the 

assembly of po[)nlatlons of Ensiiiuui \\\U) ihe current 

across ha[)lotype cdade borders, which remain as foiiii of a ring. W hereas khmhcri has nsuallv been 

the land associat^'d wilh the Salinian Block originated 

suggestions foi 

movenKMit i)\' oregouensis-Wkc salamanders soutlnvard 
gave risc! ])oth to northern pluU'iisis and to the 

logically similar forms meel they merge gcnelically, 

markers ol past distribulioual limits. In contrast, when envisioned as well-nested wilhin ihc complex, this 

morphologically and ecologically dilierentiaUxl forms alternative view (shown in Fig. 2. although the 

meel they hybridize, in eeotones in which both brandling nctw the base of the complex is not well 

parental forms are pri^sent. No indication of po>L- supported) is that xanllwpli(<j + rscliscliollzii, which 

mating isolation is found. The hyluids and back- 


I a ( 

lislincliv(* j)hylogeogra[)hic unit, might form 
crosses are hypothoized to be at an adapli\e a clade thai is sister to everything (dse, even including 
disadvantage to eitluM^ parental cla^s. ami wt' liave ihe (li\(M-se po[)ulational groups identified as orego- 

measni"e(l extraordinary 

levels of selection against 

ncjisis or picla. Some of Stebbins's subspecies are 

tlieni (ca. 46%-75%) (Alexaudrino et ah. 2007)). The liistoric-al units that can be diagnosed l)y morphology 
classic explanation by Sl(^bbins (1949) thai intergra- and molecular characters [klinihcri, xaruliopfird, 

dation oceui"s in llie north, hybridization in ihe region 

ol the' Iransvallex leak in tin- nuddle. and sympatrx in 

esclischollzil); others are either nontnonophyletic 
amalgams {j}l(Ueiisis) or incompletelv dilferentiated 

Volume 93, Number 1 


Species Formation in Salamanders 


l>L]t arhiptively diverged groups (southern plalcnsis- variation and concluded thai only a single species, B. 

crocea(ci\ picta-orcgoiiensis). Finally, orcgoncnsis is an atlcnuatus (Eschschohz, 1833), was represented in 

California. A related norlhern species, B. icrighlorum 
(Bishop, 1937), was found in the northern Cascade 



un(uagnosante gron[)nig 
braneherl independently (Fig. 2). 

of differentiated lin<'ages that 

Ensal'uia illustrates a complicated relationshij) Mountains of Oregon. Hendrickson's conclusions were 

between aflaptive divergence (as exemplified by the controversial because his two subspecies of B. 

evolution of aposematic coloralion in association with allenuaiiis occurred in complete sympatry on Santa 

mimicry in llie coastal popuhitions, and ciyptic Cruz Island, off the coast of southern California. This 

coloration in the iimer montane populations) and unusual laxonomy resulted fr 


4 4 

■om nis envisionnig 

vicariant events (for example, the difh-rentiation (»f a complex biogeogra[>liic scenario in which the island 

northern and southern plalcnsis). \^'hile oiu- under- was invaded by two somewhat (Hfferentiated popula- 

standing of the com[)lex has changed greatly since the tions. one from the north and the other from the south, 

work of Stebbins (1049), ihe basic point ihal this is estabbshing sympatry that formed from a ring-like 

a case in which adaptive divergence has been pattern of (hfferentiation (he was strongly influenced 

dominant still hob Is. This understanding does not by the work of his adviser, R. C. SteblMus, on 

help us to establish a belter taxonomy, and with the Ensatina). 

present data, no alternative seems more appropriate 

Subse({uent researcli revealed many spet:ies bor- 

than maintaining what we now have, a polytypic ders. and currently 20 species of Batrachoscps are 
species. Establishing taxonomic species within the recogni/ecL Onlv one, B. icrighlorum. is not found in 
complex creates new problems. For example, /)/a/e//.s7*,s- California. Analysis of allozymic and mtDNA data sets 

is readily diagnosable on morj)hological grounds, l)ut 

identifies six major clades, all found in California. 

not with either DNA (dipliyle(ic) or ])n)leins, and S|)ecies belonging to different clades often are so 
crocealcr, also diagnosable on morphological grounds similar morphologically that they cannot be di; 

^ ( Lscrim- 

is nested W'ithin ^ou\\\ern platens is in the DNA tree. T iiialed without molecular analysis. Tlie three members 
conclude that this is a rare instance in wliich 

of the subgenus Plelhopsis Bishop, 1937, the sister 

subspecies are helplub Tliey reflect what is in essence laxon cjf subgenus Balrachoseps, differ from the latter 
the shallowest (most recent) titne depth, related to in some osteological Irails, and while most species of 
current adaptive antipredator strategies. At an in- subgenus Balrachoseps are more slender than those of 
terme(h"ate time level are the genetic intcrclianges Plellwpsis, one {B. slebbiasi Brame & Murray, 1968) 
associated witli population-level mergers around the closely resc^nbles species of Plclhopsis. At the 
ring, rt^vealed by allozymes. Finally, the deepest le\t'l molecular hnel, however, B. sfebhuisi is sharply 
is reflected in th(^ exclusive distributions of the tliverged from Pletliopsis, differing both in allozymes 
haplolype groups recognized in I'lgure 2, all ol which (more than 10 lixed dillerences in conservatively 
have discrete geographic limits and may reflect, in evolving proteins) and in iiUDNA sequences (W^ike et 
part, allopatric episodes at different times in the past. ah, 2002). 

Along the coast ol California clades replace one 
another g(-ographically (Figs. 3, 4). The (lUcuuatus 
clade ill the north is replaced b) [\\e pacijlcus clade in 
the central coastal region, and it in turn is replaced by 
the nigriicntris clade to the south, which finally is 


The Slender Salamanders, 


genus Ddirdcnoseps, 

have a geograpliic range in California that is similar 
to that i)[ Ensatifia (Fig. 3), but in other respects tliey replaced by another member of llic pacijlcus clade in 

shaip contrast to Ensatina. Species of tlie far south. Ecological transitions between the 

are a 

Batraclioscps occ-ur in syntopy w^ith Ensatina at most borders of the grou[) are almost imj)erceptible, and the 
sites of range overlap, including a vast array of species represented are similar in morphology, in- 
cluding coloration, and ecology. Tn the central coastal 


rangnig irom temperate rani lorest ni 


morphologically similar species that once again 


northwestern California, to relatively high elevations region, the pacijlcus tdade is represented l)y four 

(ca. 2()()() m) in the forests of the Sierra Nevada, to 

chaparral and coastal sage scml) along liie southern replace one another from north to south. Furthermore, 

coast. Like Ensalifia, these are strictly terrestrial in southern California a geographical replacement 

salamanders that lay rlirect-dcveloping eggs on land. palteni is found within the pacificus clade, starting 

They are sedentary, with home ranges that are even with one species on the northern Channel Islands and 

smaller than those of /?/?.sY//z"nf/; lliere is little evidence a second on the southern Channel Islands and 

of dispersal. adjacent mainland. The most southerly member of 

A detailed morphological analysis of Bafrachoseps ihc pacificus clade, B. major Camp, 1915, has several 

(Hendrickson, 1954) recorded extensive geographic clearly tlistinguished haplotype clades within it, and 


Annals of the 

Missouri Botanical Garden 


Subgenus Plethopsis 

B. campi 
B. robust us 

Subgenus Batrachoseps 

attenuatus Group 

B. attenuatus 

nignventris Group 

D B. nignventris 
B. gregarius 
B. stebbinsi 
B. simatus 
Upper Kern taxa 

relictus Group 

B. refictus 
B. kawia 
B. regius 
D B. diabolic us 

pacificus Group 

B. fuciae 

B. incognitas 

B. minor 

B, gavilanensis 

B. pacificus 
B. major 
B. andus 

gabrieli Group 

B. gabrieli 

-. * ^ - ■ * 


Batrachoseps complex 

in California 


Figure 3. DiaUihulIon of tlu- sprcies of Batrdchoseps In CalifoiTiia. The photn^^raplis arc of s])efMnions of thr four species 
(■()m[)r-ising {\\c (Maitral loaslal cluster of the />ac[/7c7/,v cladc (photos Ijv M. Gaicfa-I'an'b tK 0. B. Vv'ake). Aulhoiitics fur species 
\vhtac uol pr()\i[lcd in the text: R. campi Mai'low, Brodc <K Wake, 1979. B. robustus Wake, Yanev & Hansen, 2002, IL kanla 
jockusch. Wake & "l ancv, l^^*)8. B. regius Jockusch, Wake tS. Vanev. 1998. 

again they replcice one anolber frotn north to south tion of 5. relidus (Sierra Nevada, eenlral Coastal 
(Wake & Joekuscli, 2000), ihis pattern appanaitly CaHfornia, Santa (>ru/ Island, and moiuitains of Baja 


■onltnuing Into Baja California (impoblished). 

CaHfornia) stimnhited Yanev (19/8, 1980) to eoiKhicl 

These patterns rai^^e questions con(^erning species an extensi\e study ol alh)ZMnes. Slie foinid inie\|)eel- 
deliinitation and eireuniseription. Because Batrdcha- 
seps atlcnuatus ((illcnuddis elade) oeeurs in sNinpalry 
with B. gavilanensis Joekuseli, Yanev & Wake, 2001 
(pacificus clade) without evidence of interbreed iug and 

witli great genetic divergence between tbem (D as lions that [?ianie and Murray considered to be B. 
defined in Nei, 1972, ea. 1 .6). two species are pres(Mit, 

edlv lare:e (h\eri^ences and hijili le\^els of variation 
within the taxa she recognized. Yane\ found that B. 
allenualus was restricted to the region nortli of 
Monterey Bay. bi the central coastal re^gion, popuhi- 

alfenualus were assigned to B. pacificus (an unnamed 

even ibotigb they cannot be distinguished in llie Held. semispecies, now B. garUancnsis). Populations from 

Other instances of s)"in[)ati*) led Branie and Murray more soutlierly parts of the central c:oasla1 region 

(1908) to undeilake a progressiv(M'evisionary sttidy that identified as B>. rcUctiis by Branie and MiuTa)' were 

was a {)relude to subse([uent research. Brainc and considered by Yanev to constitutt.^ another unnamed 

Miu'ray recognized two species in southern CaHfornia semispecies of /I /^r;n7/r//A (now three species: /?. ///r?V/e 

[B. major, on ihe mainland and southern Pacific Jockusch, Yanev & Wake, 2001, B. incognilus 

Ishnids, and 5. pacificus Cop(^, 1865, on llu' uoilliem Jockusch, Yanev & Wake, 2001, and B, minor 

Channel Islands), which they separated from B. Jockusch, Yantn^ & Wak(% 2001). Brame and Mtnray's 

atlcnuatus on morphoh)gical grounds. They also de- B. major and B. pacificus were also considered 

scrlbetl three species from the southern Sierra Neva(hi semispecies by Yanev and treated taxonomically as 

(/?, sfchhinsi. B. simatus Brame & Muiray, 1968, and B. snl)species of B. pacificus. Yanev had a narrower 

relidus Brame & Murray, 1968). The curious (Hslribu- perspective on B. rcUcius (j-estricted by Yanev h) the 

Volume 93, Number 1 


Species Formation in Salamanders 


30 mya 

mid-Oli eocene 


San Andreas 


18 mya 

Furure ■ i i * ■ 

Snn iVaiicisco iTud-Mioccne 


12 mya 

mid- Miocene 




Sur Nacimiento 



Precursor of 
pacificiis clade 



In ciae 



O PL Rc}'cs 
O iTCsno 


8 mya 

laic Miocene 

4 mya 

early Pliocene 


III ciae 
pacific us 



2 mya 



^ faults 



hi ciae 



III ciae 



-.-... -j^. 'W^fV^JiWK 






in cog nit us 





northern ^^ae*'^^_^ 




1 mya 

early Pleistocene 



lucia e 


so. major ■ 


i f 



no. major 


Present Day 

Distribution of 

Batrachoseps pacificus 




Figure I. Ilitstorical hiof^rojijraphy of llic Bainichoseps pacificus clade in soullicrn and ccnlral California. This scenario is 
based ozi geological reconslruclions by Hall (2002) and the phylogrnetic hypntheses of Jocknsch ct al. (2002) and Jockusch 
and V(^ikc (2002). 


Annals of the 

Missouri Botanical Garden 

F^oiilhern Sierra Nevada), (*()iisi(l('r(Ml to he a semispccics only sympatry between hvo nirnihers of any one of llie 

vvilliin llie/x/c'i/Iru.v e()niple\, ari(l sill' i('(luced il, L()(), l() six iiiajtn- clades is helvveeii B. nlgriveniris and II 

snfis[)e{'ilic status. The p<ipiilal ions from the mounlains sfrhhinsi, which ro-occur in the Tehachapi Mountains 

ol Haja Calihmiia were eonsidcicd to represenl a final at the southern end of the Cenlral Valley. These 

ininaincd seinispecies of />'. pacijlcus. Popuhitions on sprries dispkiy nior[>liologicaI and eeologieal di- 

Santa (aiiz Island, assigneil lo /). rclictus by Brauie and vergence, unusual anion^ ilose relatives in this genus. 

Murray, were assigned by Yanev to a resurreeti-d Tl 



te sjuaiior and !nore slender B. nigrircnlris is 

species, /?. nigrirrufns Cope, 1869. In many ways a hahilat goneralist, found in woodlands under small 

to large cover objects and using retreats in the soil. 

Yanev's recognition ol B. nigrivcfitris was her most 

im[)orlant contrilxjlion. This widespread species oc- The substantially larger and more robust B. stebbinsi 

curr<Ml in sympatry with other s|)ecies o{ Batraclwscps is rnosl frequently found in rocky soil and small lalus 

in central and soulliern t-(»aslal Cabfonn"a, on Santa slopes. These tw'o species, which are not sister taxa, 

Cru/ Island, and in the southern Sierra Nevada. It may have undergone character displacement, and if so 

turned out to be the key in unraveling the complex it is nni([ue in the genus. 

hisloiy (t( the genus, which Is more complicated than 

There are some im[)ortant exceptions to the general 

e\en Brame and Murray had conceived. Of special rule in Batrachoseps dial >pecies either replace one 
inU'rest was the complex [)attern of range overlap widi another without hybridizing or are sympatrie. In 

no sign ol hybridization or genetic leakage of 




ornia, where pojiulation density is low% 
morj)hol(»gicaUy cryptic species in the Tuner CoasI [>oj)ulalions of "northenr^ and "southenr B. major 
Hange in central California, where B. aUeniiatus and diat are morphologically identical have nUDNA (cyt h) 
tlu^ (airrent B. gavilaneiisis were narrowly sympatrie in genes that are about 9% (h'\'erg(M| and are not sister 

(Wake & Jockusch, 2000). In fact, mtDNA of soutlun-n 

narrowly sympatrie in the south. In coastal central />'. ///^//"^>r is more closely relah-d (o /?. /;ae(//eu5, a mon^ 

robust species that is morj)hological!y distinct, than to 

the norlli, and B. gdi'ilancn.sis and B. nigriventris were 

Calih)rnia tl 

le geographic range ot U. attenuohis 

f B. 

overlaps that of B. garilanensis, whose range abuts northern B, major (Fig. 1). However, northern and 
that ol B. luaae. Parapalry, but as yet with nt» range soutlu^'n populations are only slightly differeTitiated in 
overlap, occurs further south Ix^ween B. luciac and B. 

proteins, and \\'ake and Jockusch argue diat when 

ificogaiUis, and B. incogmlns and B. m'nwr (Figs. 3, 1). diey mvv[ secondarily and inleract genetically, alleles 

(rom northern popnialions spread over southern 

However ihe rang(^ o( B. nlgriveniris overlaps dial of 

both B. inrngnitus and B. minor, witli local sympatry, populations, but the interactions have been insuffi- 

and die northvvestern-mosl range limit ol B. nlgriveniris 
is within a few^ km oi llie southern-most rangc^ of B. 

cieni as yet to dislodge the mateMiially inluMited 



souincrn mitociiondrial genes. This situation is 
reniiniseenl of Ensatina e. platrnsis in the central 

The addition of mitochondrial gene sequences and and northern Sierra Nevada (see above). 

the reitilcrpretation of unpubbshed data gathered by 

The apj)arently nonadaplive radiation c){ Bairaeho- 

Yunev (1978), as well as recent discoveries \n the seps results fi-om the complicated geological history 

field, led to further taxonomic revision (e.g., Marlow et of California (Yanev, 19i5(); Jockusch et ab, 2001). 

ab, 1979; Wake, 1996; Jockusch et ah, 1998, 2001; Tlu^ first split, an ancient one, was h(Hween UKan- 

Wake et ab, 20().'5), summai-i/(Ml by Jockusch and hers of subgenus Plelhopsis and sul)genus Balraelio- 

Wake (2002). The distribution ol species and tlu; seps. Today Plelhopsis is located peripheral to 

inf<a-r(M! juitlern of species forrTiation is what Gittt^n- Balraehoseps, to the north and east of the main range. 

berger (1991) termed tionada[)ti\ c radiation, pliyloge- Within subgenus Balraehoseps die fiist split segregat- 

netic diversilieation not accom|)anied l)v adaptation ed B. alfenuatus frnm eyer\\h\\v^ ehe. The aKenuaf us 



species, IS 

into (hsiinctively different ecological niches (see also clade, with a single but difft 

Wiens, 2004, who refers to ecological niche conser- distributed mainly northeasl of die San Andreas Fault 

vatism). The result is a group of allopatrie or zone and north of the historically significant (^mbay- 

l)arapatric species, with the parapatric forms Isolated ment of the Central Valley in llu^ vicinity of prestail- 

;eographieally because of inferred competitive inler- 


y Montei-ey Bay. The relletns clade, perhaps tin 

genetic di\('rgence are sulficieni to preclude in- 

terbreeding; or hvhridi/ation, and the eeolosieal 

aeiioirs at borders of species ranges. The levels of next to ])rauch phylogcnclicany, is restricted to the 

Sierra Nevada and western adjacent lowlands. It 
dl^[)h^ys a distinct pattern of regional displacement, 

similarities are sufficient to maintani largely exclusive with substantially more divergence than wilhin 

distributu)ns. the alienuatns clade. Four species are recognized, 

A general feature of \he no[iadaplive radiation in each occupying an exelusi\e geM)graphic range. The 

Balraehoseps is the relatively limilf^l sympatry. Tlu^ nordiern species, B. diaboluus Jockusch, Wake & 

Volume 93, Number 1 



Species Formation in Salamanders 


Yanev, 1998, split fnun the reiiiainiiig species in and mlDNA diversity ^vithin the northern clustt^r of 

the vicinity of ihe mi(hSierran glacial region, a region extant species in the pdcificiis clade. 
in which there are north-south s|)lits in diverse taxa. The next species to sp]it (Fig. 4) was present-day 

The remaining clades, gahneli. lugrivejitrls, and Batniclioseps luci(i(\ which now occurs on a plate 

pacificns, arc kirgely southern, with gdhricU isolated fragment (Jockusch et al., 2001). After the first two 

in the soutliern transxcrse ranges, nigriventris con- spUts our phylogeny is less rohust. What is ch^ar is 

centrated in die souduMn Sierra Nevada, Tehachapi that eacli of the central coastal species is sister not to 

Mountains, and some more soudierly and westerly its nearest geographic neiglibor hut to some complex 

extensions, mid pariflrus located in coastal regions, of poj)(dations to the south. Thus, 5. /K/.ci/Icu.s a])])ears 

extending from nortlicrn Raja Cahfornia to just north to ha\ c been the next [n move north, and out to sea, on 

of Monterey Bay, south and west of th(; San Andreas the precursor terrane diat gave rise to the jiotthcru 

Fault zone. Chann(d Islands, l)ecoming isolated from populations 

The onlv clade that crosses the San Andreas Fauh on die mainland. Progressively, B. inrognitus and B. 

zone to any degree of significance is nigrireutris, and mijjnr were transport<'d north\vard. leaving a compli- 

in particular BatracJiuscp.s nigrivenlris. a species that catcd B. major in tlu^ south dial is made up of several 

lias violated the range exchisiveness so characteristic distinctive phylogeographic units, essentially left over 

of the genus to establish [)opulations sympatric widi from episodes of isolation. The northern ph)logeo- 
members of the /)r/r//7r//,s chide along die central and gra[)hic unit within B. major either has or is in the 
southt-rn California coast and on the Channel Islands. process of extending its range south and east, where it 
This tcixon (hsplays greater ecological breadth than appears to be merging genetically with poindaiions 
any other member of lh(^ genus and likely represents characterized by non-sister mtDNA haplotype clades, 
an extensive and relatively receni range expansion morphology, or both. For example die problematic B. 
from its origin, inferred to be near lh(^ southern end of aridus Rraine, 1970, variously recognized as a sub- 
the range of its sister taxoii, B. gregarius Jockusch, species of B. major or as a full species, is closely 
Wake & Yanev, 1998, in the vicinity of the Kern related to a southern phylogeographic miil of /J. ///ayo/-. 

^\\\c pacificus cladt^ displays at a fine scale what I 
consider to be a long-sustained |)atterii of nonadaptive 

Ftiver, where so much of the evolution of the 
nigrireutris and rellclus clades has been centered. 

T\w pacific us group has l)een more affected by the radiation in Batrarhoscps. An ancient lineage frag- 

massive land movenu^nts that have taken place west mented again and again, with a resulting patchwork- 

and south of the San Andreas Fault zone than any of quill pattern of lineage segments, i.e., species, that 

the otlu^r Batrachoscps. The scenario develo})ed by general l\ show ^lighl stitching,'' close parapatry with 

Jockusch et al. (2001), based on their mtDNA no li\l)ridi/ation. Some restricted sympatry occurs 

phylogeny, envisu>ned an origin of the lineage in between members of dilTerent major clades, which in 

southern California. A new geological reconstruction the cases of B. mgrlvenins an<l B, gregarius is more 

of coastal California (I lall, 2002) has enabled a hnlhcr widespread and involves more than one otlier taxon. 

develo[)men[ of the scenario (Fig. 4). The first split 

Why the nonadaptive radiation in Batrachoscps 

separated the pacificus (dade from a nigrircniris or resulted in a patchwork-ciuilt pattern of distribution 
g-a/;n'c/i ancestral sister taxon, with the />ar(//c//.s clade requires closer examination of the history of the 

associated with the Pacific geological plate in the central coastal region. The four 

species o 

f tl 


paleoterranc known to geologists as Salinia. Tliis may 
have occurred as long ago as about 30 million years. 


with earlv sta";es of the northwestward movement and 

geographic ranges, and they are ver>^ similar in 

Since Oligocene, extensive land movements have mor{)hology and ecology (Figs. 3. 4). Two of these, 

transporti'd pieces of tlu^ continental crust associated B. garilanensis and B. luciae, occupy relatively large 

with Salinia more than 160 km to the nortluvest. 41ie areas and have sufficient samples to disclose 

first sj)lit \vithin the pacificus c4ade w^as associated significant geogra|)hic and genetic variatirai. 41iese 

two s])ecies show extensive geographic variation in 

fragmentation of Salitua. Today the northernmost bodi allo/ymes and mtDNA ha|)lotypes. In fact, the 

member of tlie pacificus clade, B. gavilancnsis, is dilfer(Mices within each approacJi the level of 

the only species to lia\e [)enetrated territory north of differciice betAveen thcni (Jockusch et al.. 2001). 

the ancient Central \ alley embayment, in the vicinity Yet, in the border zone where the ranges of the two 

of present-day Monterey Bay. Its penetration north- species abut, no syntopy or genetic interchange is 

waifl, [)rol)ably a relatively recent event, has estab- detected. Genetic distances across this border remain 
lished a zone of sympatry with B. altcnuatus. As one 

would expect for a relatively old species, B. conip 

hidi. AN ilh some (ixed 


ozvmic ddferences anc 


Icte segregation of mtDNA haplot)pes, but no 

garilanensis shows the greatest degree of protein 

ecological differentia I ion 


IS ouserve 



Annals of the 

Missouri Botanical Garden 

T\\r patchwork pallcrn, wliich is general in tlie potential mates. In llu; ease uf salainanthuvs, lliis is 
genns, likely arises IVoni several factors. First, tliese most likely to involve mating pheromones (Ilonck & 
salamanders are extremely sediaitary, with limit<Ml Arnold, 2003). Postulated [tremating isolaling inech- 
dis|)crsal. Second, today's species represent lineage anisms rnighl l>e incidental, a l)v|)roduc[ of the 
fragments of fornuM- species, which themselves were 
eograjtliiL-all) tiinerenlialcd. Tlius species are "Ijoro"" 
with gcogra[ihic varialion. Third, species, especially borders of two incipient species, it is vcrj" difficult to 
clos(^ rehui\es within a tdade, re[)lace one another 

<.H((erent genetic histories of lineages since time o 
di\ergence, II isolating mechanisms did arise at tht 






imagine a scenario in which they would spread 
"haekwards" ihrnughoul the fai'-flnng populations of 

geograpincaiiy ixK-anse Uu^y are so snmiar ecologi- 
cally that theie is what ma) he called preemplive each s|)ccies, which are so genetically helerogeneons. 
occupancy of s[)ace. Tlial is, []\c space-holders ha\e In such situations ihe e\'olution of isolating mecha- 
relatively large and widl-cslahlished popidations thai nisms seems imliktdy to l)e related direclK to the 
resist in\asion by others llial are virtually idenlical fonnalion of species, 
ecologically. Wiens (2001) has discussed such niche 
conservatism and considers it to be a major facloi in 
the fonnalion of similar species under allopalric 
conditions. Areas where populations merge with 
others having non-sister ha])lotypes tyi)ically ai(? 

Ci:m:ha[. Discission 


The contrasl between PxilrncJioseps and F/isadrui Is 
great. Where mor|)hologically and ectilogiealK similar 

ecologically marginal, with [)opulations scattered 

po()ulalions of EiuuUina meet ihey exchange genes, 
and small. Under sucli circumstances, populalions whereas in Rdlnichoseps they do not. Wliy does this 
may have very low densilii's. and Individual organisms stark contrast exist? The two genera ludoiig lo ihe 
that meet may have few mating ()|)portunities other same major clade (TIethodontidaej. have sitnilar life 

than with heterospecilic individuals. 

histories and (x-ologics, and species of llie two are 

S)nipatr) l)etween sp(H*ies is fiamd in two conlra^l- often svmpaltic. Roth are fulK tia-reslrial. However, 

^ 1_ ^ V 

Ing si I ua I ions. The first is whiat; there is 


Enscitina is a lari^-er salamander, wilh bell(M- loeomo 

tory ability and larger I 

lome ranges i^eom[)are 


ecological divergenc(\ oflen related to dinerentialion 

in ihe bod\ sizes of the Iwo species. Exam[tles include Stebbins, 1954, and Slaiib et al., 199rx wilh (annnng- 

Rdtnicliosrps major wilh H. uigrivcuhis, B. nigrlvriilris liam, 1960, and llendrlekson. 1954). Bolh genera are 

ith B. .slebbinsi. and /?. nii^riicnlris wilh B. Linhrieli f)livlot^encticall\ isolated, haviii"; no (dose relatives, 

W ak(\ 1996. The second is in areas where the ranges and likely rc[>rcscnt \ery tdd lineages (perhaps on the 

(►f s])eeies become (Hsconliuuou^ and where jjopnla- order of 60 iiullion vears or more, based on estimates 

tiotis are liighl) localized. This is ihe sitiialion in the from rates of albumin evolution and degree of 

di\ergenci: in m|[)NA and other data. e.g.. Larson et 

genei'ally inhos|)itable Inner Coast Range, a lai'gcdy 

treeless area with exceedingly hoi and dry summers al., 1981, 200.5; Chippindale et al., 2001; 


and I it lie winter rain. 1 1 ere l)road 

)roa(i regional ranges 

2005; Mueller et al., 2004). Batmchoscps is tlu^ more 

overla[), but liltle or no local syntt)py is found, as in Internally di\('rged and differentiated, and is likely 
the eases of/?, attcundtiis and />. gdvilaucusis and II ihe older, lis lower vagilitx, fidelit) to pieces of the 

planetar) crust, and inferred gn^al age may be 

garHdncnsis and B. ffigrircnlris. ddiis is the same 
ecological situation in which genetic mergers mav 
take i)laee. One can only spceulate that the iiitcra<iors 

responsible for die 
lineage and wlial ha; 

fragmentation ol ll 

le primordia 

been maijily a nonadaptive 
thai (ad lo merg(^ have been separated sufficiently radiation. ^Hie j)r(teesses involved in differentiation of 
long (as estimated bom allozymic genetic distanc<'s Balntclwscps appear lo be largely relaUMJ to factors 


(k^griM^ of hapl()t\pe divergence) that geiielic 

isolating mecdianisms have arisen incidental to di- 
verst^ genelie pi'oeesses during the long 

associated with earth history, especially crustal 

mo\ements, as fifsl |)roposed by Yane\ (lOJJO). In 

period of contrast, Enscili/ui appears to be re^[)<)nsl\e lo 

geographic ist>latioii. 

challenges from its 


ogical communllv and has 

The main feature of a nonadaplixe radiation, then. e\olved sexcial different anlij)redati)r mc[:duuii>ms 
is ihe general impression of allopalry or parapaliy whieh lu 

with a la<'k of ecoloi-it a 


or an\ o iier 





ue conccHiiItanI beha\ioral and ecological 
f consetjuenees. The result is a differenllaled. but 

divergence other llian in molecular Iraits. In siluations 
like this, where there is little or no hybridi/alion, il 
may be fruilfnl lo investigaU' the evolution of isolating 
meclianisms, which might lia\c arisen IncidenlalK in 

incompletel) Iragmcnled and very widespread. iiu4a- 
po[)ulalion slruclnr(^ 

Roth examj)les have strong geogiaphic components 
lo their hi>loiics. Most sj>ecies formalinn in terrestrial 
alhtpalr) but ser\ e now lo cau>e individuals Irom xertebrates appears to be geographic in natnn\ as first 
adjacen! populations uol to (-(^'ognize each other as 

generalized by Ma\r (1912). Geographic varialion 

Volume 93, Number 1 


Species Formation in Salamanders 


wiLliin living [riTestrial verlebrale species (as well as 
many olher laxa) in natural populations is nearly 

15iologisls will eonlinue lo liave prohlems with 
species. We may all share llie same conceptual 

ubiquitous (e.g., Avise, 2000). In tlie taxa I study, there framework, but it is safe Lo [)r(Hlict that arguments 

concerning thresliolds atid attributes will continue to 

h di 

is so nuien (iivergcnce wnnm species tnai oniy 




atlaptiveiy significant alleles or allele conii>le\(^s are produce controversy. Howe\(M-, regardless of taxo- 
bkely to spread broadly and rai)idly. Accordingly, nomic treatment, careful anal) sis of patterns and 
Ensalina has experienced spread of adaj)tively signif- processes associaled with species formali<tn will 

icanl trails, and lliis has kept the lineage from 
peiTnaufMit fragnifMitation. ffowever, in Bdtrachosrps, 
where no (dearly adaptive traits beyond those general lo Liiriiinirc Cited 

inform meaninglul discussion and debate. 

most species have been identilied, divergence and 
lineage fragmentation lias proceeded. 10 h)cus atten- 
tion on ihe evolution of isolating mechanisms in 
situations like this is problematic. When long-se[)arat- 
ed populations that have diverged signilieaully come 
into seconcLiry contact they may l)e sndicienti) (hstiuct 
that die\ no longer recognize cacli olher as potential 
mates (e.g., Ko/ak, 2003). I suspect that diis has 
happened in BaIracIio.scps, where one never finds 
hybrids, but instancies of ha|>]oty|)e para[)liyly and 
polyplnly arc found, suggesting thai secondary contact 
was h)llo\\ed by genetic merger (cf. Fiuik & Omiand. 
200."?). Ah<'rnatively, offspring produced in such 
contacts may be adaptively inl(;rioi. Fliis is the case 
in the adaptively (hlh^-eut Ensdlifui in the cential 
Sierran and soulliern California Inbrid zones, uhich are 
onlv a few home-range diameters wide. One mi<iht 

Alcxaiidritio. J., S. J, K. Baird. L, hawson, J. H. Macey, C. 
Moril/ & D. n. \^'ake. 2005. Strong sclrction against 
li\l)rids at a li}l)ti(l zone in the luisatina ring species 
coiriplex and its evotiilionaiA implications. E\()luli<)a 59; 


vVnipliihiiiWeh: Information on ainphihian biology aiul con- 
sci-\ation [\vcIj applicalionj. 2006. Rerkeic), Catifornia: 
Anii}liihia\\ ft). A\ ailahh^: <hll]»://anipliil)ia\vch.(>rg/>. 

Avis(% J. C. 2000. l^hylogcogrci|)li): The lli.slory and 
Fornialion of Sptxaes. ftarvard Uni\. Press, Caiiil)ridge, 

Brainc, A. H. Jr. tS. D. B. Wal^e. 1962. A new s]>cLies of 
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& K. F. Murray. 1 96G. 


riiree new slender 

.-^ahmiaiiders {Balniclioseps) with a discussion o( rctalion- 
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llir plclhodonlid salanuuulei' Ef\S(ilina escliscliolizii. Univ. 
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Bush, C. [.. 1969. S\inpati[f host race formation and 
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Chippindalo. P. T., U. M. BonoU. A. S. Baldwin ^ J. J. 
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study isolating mechanisms in these instances, but 
genetic isolation likely (nolved incidentally during die 
allopalric (h\(n"gences, not upon recontact. Perhaps 
hybrid zone or alloparapalric interactions (Alcxandrino 

et al., 2{)()5) are settings in which the potential 

reinfoi-cement of isolating mechanisms might be 

studied (Serxedio & Noor. 2003). C/COgraphy is die 

common theme, ^^■hc[hcv species formation has pro- ^^^^^^^ j ^ ^ ,,^_ (j,.^,_ 2004. Sp<Tialion. Sinau.-r. Sund.M- 

land, MassaohuscUs. 

Cracrafl, J. 1989. Specialion and its onlulog) : The empirical 
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. 1997. Species conecpis in sysleniaties and tronser- 

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S[)ec ies: The Units of Bio(hversity. Chapman iK Hall, 

gressed ada[)lively oi^ has been Incidental to events 
related to isolating mechanisms. 

Al what le\el of lineage segmentation do we recognize 
and name species? Rex-ently de Qiaaro/ (2005) [)ointed 
out diat while the process of evolutionary di\r'rgence leads 
to die ai(|uisition of (hderenL properties by diverging 
lineages, taxonomists differ with respect to which 
particrdar propeit) the) emphasize. I le argues that the 
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tliresholds lor die two examples jiresenled here, but have 
reached veiT different conclusions. De Oueiro/ argues that 
"all sej)arately evob ing mcta[)Opulation lineages would be 
species" rt^ganlless of |)arlicular attributes, but in the case 
of Eus(i{in(K for example, the issues of separateness and 
metapo|)ulalion limits remain unclear. Ihe likelihood that 
once separate lineage segments are now genetic-ally 
merged, or lia\e in tire I'ccent jjast midergone sccondaiy 
genetic merger, is high. In contrast. In Balrachoscps the 

on. Pp. S7 

/o in 

Pacific Slender Salamander, Bdlrachoseps pacificus, in 
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de Oueiroz, K. 10')8. Ilie general lineage concept of speci(;s, 
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. 2005. ErnsI Mavr and tlie modern conc(^j)t of 

same issues are more gener'auy reso[\f'( 



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Jackman. T, R. & D. B. W'akc. 1 99 L Evolutionary and 
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J.»ckusch, E. L. ^ D. B. Wake. 2002. Falling apart and 
merging: rji\ crsification of slcndta- salamanders (Plrdio- 
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Columbia Lui\. Press. \ew York. 
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relation --hips within the Ensaiina csrhschnllzii enmph'x 

confirm the ring s|)ecies inler|)r(Matioii. S\>t. /ool. IL 


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(ialifornia. Brrkeiew 

milocl loud rial genomes. Proe. 

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200 k ^^l^p]lologieal homoplasy. Ii(e lus!<ir\ evolution, and 
hi>to]ical biogeogr-aph) of plrdiodontid salamanders 
inferred fi-om comj)lctc 

iXatl. Acad. Sei. MIL 13820-13825. 

Nei. M. 19(2. (/cnrlic distance between |")opulatio!i>. \tucr. 
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Parks. D. S. M. 2000. Ph\ logi^ograpliN . Ilisloriral Distribu- 
tion. Migratujii. and Species Boiuakuies in die Salamander 
Ensdiina csclischalfzii as Measured with Miloehondi-ia 
DNA Sequenc(\s. Ph.D. Tlie.^is In Integral iu- Biology, 
Lniv<-rsitv of (^alifornI;i. Bri-kh->. 

Serv<-dio. M. R. X- M. A. F. Noor. 2003. Jlic role of 
reinforcemeni In speciation: llieory nnd data, \nnual Kev. 
Eeol. F^ol. S^sl. 31: 339-36 L 

Sites. J. W . Jr_ cK J. C. Marshall. 200 1. Operational eriteria 
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D. R. Wake & K. P, Vanev. 1998. \ew species of Staub. N. L.. C. W. Brown .^ D. B. Wake. 1995. Palt.-rn^ of 

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Nat. Mist. Mus., Los Angeles Co. 472: 1-17. 

';:ro\vlh and mo\'emenls 


-, K. P. Yanev & I). B. Wake. 2001. Molecular 

ph\logenelic analvsis of Sieiuln- Salamaiid(a"s. ircnus 
Balrachoseps (Amphibia: Plethodontidae), from central 
coastal C^aliforrn'a with descriptions of lour lu-w species. 
Her[)etological Monogr. 15: 54-99. 

Kozak, K. H. 2003. Sexual isolation and courtship beha\ ior 

a pttpuhit ion of hnsalina 
c'sclischolfzn f)l(ilc{isis (C^andala: Plethodontidae) in tJu- 
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ph-diodoutid gfMius Ensttlina. Vi\'\\. Calif. Pnbl. /ool. Ml: 

. 1954. Nalui'al [n'stor\' of I lie sahmiandrrs of the 

|4ethod(mlid genus Eiisahna. \}\\\\. (ialif. Pnlil. /(tol. 5L 

in salamanders of die Eurycca bisJiiwaUi speeies conij>le\, Tejiiplcton, A. IL 1989. Th( 

with commenis on th<' evolution of the mental gland and 
pheromone deliveiy behavior in thr Ph-thodontidae. S4-7 
Naturalist 2: 281-292. 

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meaning of specie.s and 
spec lation: A genetic pcrsjjei'ti\ i'. P[). 3-27 /// D. Otl<- tK 
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473: 1-12. 

Volume 93, Number 1 


Species Formation in Salamanders 


. 1997. Incipient species fornialion in salaniamlcrs of 

ihe Ensiiluui complex. Proc. Natl. Acad. Sci. Ok 


3^ \\. L. Jockiiscli. 2()(){). Detecting species bor- 
ders using ili verse data sets: Plethodonlid salamanders 
in California. Pp. 95-110 /// R. C. Bruce, L. Houck & 
R. Jaeger (editors), The Blolog)' of die Pletho- 
dontidae. Klnwer Academic/Plenum Publishers, New 


& C. J. Schneider. 1998. Taxonomy ol die 

plethodonlid salamander genus Ensalifui. n(?rf)etologica 

54: 279-298. 

& K. 1*. Yanev. 1986. Geograi)hic variation in 

allozymes iti a ^'ring species," die plethodonlid salamander 
Ensaliiia esdischohzii of vveslern North /Vnu-rica. Evolution 

40: 702-715. 

, & C. W. l^rown. 1986. Inlraspecific 

sympahT in a ''ring species," th(; plethodonlid salamander 
Ensalinn cscli.schollzii, in southern California. Evolution 

40: 866-868. 

hybriinzalion in a 


& M. M. Frclou. 1989. Sympatr\' and 

species": The plethodontirl 
salamander Ensalina e.^cbsrholtzii. Pp. 134-157 in D. 
Olte & J. A. Endler (c(h lois), Special ion and Its 
Consequences. Sinauei'. Sunderland, Massachust^tts. 

& R. W. Hansen. New speci(\s of slender 

salamander, genus BafrarJu)srps, from the southern Sierra 
Nevada of California. Copeia. 2002: 1016-1028. 
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Phylogenetic niche eonservalion and the origin of species. 

Evolution 58: 193-197. 

Yanev, K. P. 1978. EvoluliouMry Studies of the Plethodontid 
Salamander Genus Batrachosrps. Ph.D. Thesis in Zoology, 
University of California, Berkeley. 

— . 1980. Biogeography and distribution ol thr(M.' 

parapatrie salamander species in coastal and borderland 
California. Pp. 531-550 /// D, M. Power (■edilor), The 
California Islands: Proceedings of a Mullidisciplinary 
S)niposIum. Santa Barbara Museum (jf NaUnal Histor)-, 
Santa Barbara, Calilornla. 


JoiKifhan />. Losos, Richard E. Glor. Jason J. 
Kolbe, and knslen Nu:hohon~ 


CiiriMn-aii Anolis li/aids aic m classic case of adaplivc radialiim, fcpcnhMl fmii- times across islands of ihc Greuler Antilles. 
On cacli island, \('f) similar pallcrns of evolulionai) divci-^ciicc liavc occiirr-cd. result iii<^ in llie evolulion ol the same set of 
ecological speclalisls — termed ocomorphs- — on each ishuid. Huuevcr, diis is onl) pait of ihe ^[or) of the Carihhean anole 
radiations. hidiMMJ, nincli (»f Mie species diversity of Carihheaii Anolis occnrs williin ehuh'S of ecomorphs, which contain as 
ntany as ]\ ecologically-similar s[)ecies on a single island. WV ask lo what cxlenl the chissic model of ecological inleraclions 

for-ce in adapllvc radiation can account for' thi> aspect of anoh^ evolutionary d!\'ei-sil\. Our ans\v(a- is lliat il can in 
part, l)ut no! entirely. More gcnerall), the most conijihTc understanding of c\ohiiionar\ diversification and radiation it 
achievcfl hy studying tnnlll]>le hierarchical evolutionary levels from <']ades [o ]>opulations. 

Key Honis: adaptive radiation, \nolis. Carihheau. ecomorplis. li/ard. speciation. 

as the (hiviuj:; 


A(lapll\(' radialioii is ''e\'(>ltilionafy divergence of adaj)le(l lo a <liff(;i-i;iil part of the en\ ironineiit 
nK'TtilxM's of a single [)liylogenelie line inio a van(dy of an a(hi])ti\(' radiation. 


(liKorenl adanlive forms" (Ku[n>nia, 1998). Models of 
adaptive radiation (Simpson, 1953; Seldnter, ; 

begin willi a sp(^(des ifi an ein ironment in whicdi 

IJolh the (hdinition of adap(i\'e radiaUon and tln^se 
mod(ds say nothing ahoni the species richness of aw 
adaptixidy-radialing tlad(\ Indeed, such (dath's mav 

resuuretis are i)]enliliih luil few, if any. other species nol he ri( li in s[»e(des, despile their ecological an* 


are present lo use ihem. Sncdi a sitnation could occur phen(ity])ic disparity. I^^xamples of adaptive radiations 

vvilh inie\ee[)liona] spe(des ritdmess intdnile Darwin's 

in a nnmlier of ways, such as colonizaliun of a new 

JD oe 


area, evolnlion of a trail that allows the species to use fincdu^s ((iranl, 19}J6), pygopodid lizards (Wei 
resources [)i-eviously inaccessihlc lo all species, or Shine, 1991; J(annngs et ah, 2()();5), and poslglacial 

lake iish (S(ddiiler, 1996). NotKdhtdess, many oilier 

sin'viving a mass extinclioti. dhrough time, two things 
ha|^p(^n: spe(d(^s prcd derate and resources become 

adapt i 

\(^ r 

a( ha I ions — e.g., Ri(t Lake cicldids (Ver- 

nnly later do resonrc(^s become limiting — this seems 
to b(^ the model Simpson (195*5) had in mind. 

linnling. In s<Mne scenarios, specialion occurs first and heyen el ah. 2003), passerine birds (hovette & 

fiermingluun, 1999), Hawaiian silverswords (Baldwin, 
1997)— exhibit nol oidy greal ecological and pheno- 

Allernalively. in other mn(hds. resource limilation typie dis|>arit\, but also exceptional species ricdiness. 

oeein-s first, thus drixing sp(H;iation (e.g., Orr & Smith, This sp(xdes richness is generally nol obtained by 

1998; Dicekmann (5. l3otd)eb, 1999). In either case, adaiitation to an extraordinary variety of different 

(Mu iromnents, bnt rather Ijy the exislence of sets of 

however, the main point is eh^ar: speci(^s (or 

sul)popnlalions of one iidlial sju-eies) aller their species that are eculogicall\ similar, with each set 

behavior and habitat nse to pail i I ion resoin'ces, adapt (m1 to a different part of the environment. 

?)nnimi/itig eompelilive interactions. Over lime, the 

species (or snl>|)opulations) evolve features to increase 

their adaj)talion to tludr new uIcIk^s (i.e., characler 

displacement oecairs). Tn tins scenario, tmdtiple, 

[)ossibly simultaneons. instances of character dis- 

Underslanding the genesis and maintenance of this 
divejsily obviously re([nires a more compliealed 
moihd than the sinijdc model of speciation and 
(diaracler displat:enu'nl just discussed. 

rh(^ goal o( tin: 

s [)ap(M' IS to exannne one spc< h^s- 

l)lac(Mn(Mit (Misn(\ llie end-resuU is ihat a single ri( h a(ki|)tiv(^ radiation, Caribbean li/arJs In the genus 
species has given rise to a mnnl)er (jf s|)ecies ea(di Anolis Dandin, 1802. Hy doing so. we hope, first, lo 

' We thank K. dt^ (^)ueiroz, T. jaeknian. and A. [.arson, who have collahorated on much of ihe work sunanarizcd \n this 
article, 'V\)c W(ak r(^porled here was sup[^orIed hy grants fiotn the National Science iMiundation, the Xational Geographic 
So(.ael\', and the David and hueile Packard hVunidation. anions otluas. 

"Departnieut of bIolo^>. Campus Box 1137, \\"ashin<^ton I iiivia-sily. Saint l.onis, Missouri 63130, U.S.A. iosos((^^ 
hio!og\ .wu^tl.cdu. 

Ann. MissoiKi T^oi. G\ui). 93: 21-33. Pi busiifd ()\ 31 M \^ 2006. 

Volume 93, Number 1 

Loses et al. 
Caribbean Lizards 


explore wliether the classic model of adaplive 

radialioii can 

adequately explain the ecolo^i^ical 

Tahle 1. Niiinhers of Ariolis species of eacli ecoinorpli 
lyjie on each island in the Greater Antilles. 

diveisifiealion of Carihhean anoles and, second, to 

examine the determinants of ll 

richness of this i'adiali(jn and 

these determinants are related to the patterns of Gniss-hush 

le great species 
investigate whether 



Hispaniola Jamaica ruerto Rico 




adaptive ddferenliation. 

Trial k 
Trii 1 1 k 










Till- Evol.tTiOXARY livniATtOXOF C\Klli[a::Ai\ A\()i.t:s 










I wig 











hahilat specialists have evohcd on only one island. 

The lizard genus AiioIls is ont; of the largest g(aicra 
of vertehrates (and the hn^gest of amiiiotes). with well Oilwv/ 
over 300 described species, 154 of which occur on 
islands in the Carihhean (Nicholson et al., 2005). Of 
partienhir interest are the anole faunas of the ishmds 
of the Crealer Antilh^s (Cuba, Hispaniola, Jamaica, 
and Puerto Rico). On each of these islands, typical 
comnuuiities contain a number of species, each oi 
which is mornholotricallv distin(4, behaves dilferently, 
and uses a diffcrenl i)arl of ihe slrucluial habitat (e.g., 
on broad surfaces near llie ground, on twigs, in gra.-r^.-^y 

areas). Detailed functional and behavioral analyses ^' (Chamaelinowps) barbouri Schmi(U, 1919 
support th(^ hypothesis that the morpliological dilfcr- Hispaniola, among others. In some cases radiation 
encesb(4\veen the species— in traits such as hindbmb lias occurred subsequent to the evolution of such 
length and toepad si/.e — are adaptations to the >i)ecialists; for example, four large species on Cuba 


lude tl 

se unique tvpes uiclude the senu-aquatic 
streamside Anolis vermiculadis Dumeril & Bibron, 
\KM on Cuba, the rock wall s[)ecialist A. bartschi 
Cochran. 1928 on Cuba, and the leaf-litter sjiecialist 


functional d 


demands im|>osea ijy ii\ nig m 

'd bv li\ i 

different (formt^rly comprising the genus ChomaclcoUs Cocteau, 
parts of the environment (e.g., Trschitk et ah. 1996; lo3o) are particularly slow-moving species special- 

Larson iJv Loses, 1996; Elstrott cK Irschick, 200 1). 

ized for narrow perches high in the canopy, and may 


The most striking aspect of Uiis diversity, however. prefer to feed on molluscau yn'cy (Leal & Loses, 2000). 

is its rci)eated occurrenc-e across all four Crealer All tnhl. 21 such unique specialist species exist. 12 on 

Vntiilcan islands. For the most ])art. the same set of Cuba. 8 on nis[)atiiola, 1 on Jamaica, and none on 

habitat six'cialists — termed 'Vcomorphs" and named Puerto Rico (Table 1). 
for the j)art of the liabilat in which they arc u^uall) 

found (W illiams, 1972. 1983) — recurs on each island. Moi.rci lAR Pnvi.oct.MTU: Pt:iisinxTtVE 

Ll all, there are six ccomorj)hs: trunk, trunk-crown, 

trunk-ground, grass-bush, twig, and crown-giant, hoiu" Recent tii()l<H:ular studies have provided a phylog- 

are foutid on all four Islands, whereas grass-bush eny h)r most of tlu^ species in the entire Caribbeati 

atioles are absent from Jamaica and trunk anoles are radiation (Jackman et ah, 1999, 2002; Creer et ah, 

onlv found on Cuba and Hispaniola. Ph\ loi^cnctic 2001; Schneider et ah. 2001; Clor et ah. 2003. 2005; 

analysis of morphological and molecular data confirms Harmon et ah, 2003; Branthey & de Quciroz, 2004; 

Williams's pre-cdadislic conclusion (1972, 19(!3) that Poe, 2004). The nujst recent phylogeny (Nicholson et 

the ecomorphs are liah^pendently th-rived on each ah, 2005), based on sequence from a 1.8 kb region of 

island (Lo-sos et aL, 1998; Poe, 2001). 

mitochondrial DNA h)r 132 (jf the 154 Caribbean 

Two aspects of the ecomorph story have received species, provides the ability to thoroughly examine the 

relatively little attention in th(^ \cars sine 

e WilMaTns 

Caribbean anole ratiiation, including both ancient 

(1983) classic re\i(^w. First, the ecomorplis are events deep in the tree and many of the more recent 

divergences. This examination reveals three patterns 
of interest that characterize anole evolutionaiT <h- 

represenl<'d on each islatid, not UfM-essarily by a single 
species, but sonielinu^s by many. At \\\v. cxtrenie, there 
are 14 trunk-groimd and 15 grass-bush species on yc^rsibcation in the Greater Antilles (big. 1): 

Cuba. All ecomorph types are rcprcs(Mited h) wun'c (1) Ecomorphs have generally evolved only oiirr on each 

than one species on at least one island, and al least '^haid. (a\'en that each eccunorph has evolved on 

I ] I , I ■ I multiple islands and that uuilliple rortrt'scnlatives of 

two truuK-grountl and trunk-cnnvn species are present ^ ^ ' 

on all islands (Tahh' 1). 

Secoti(h in addition to the ecomorphs that have 
evolved repeatedly on different inlands, a iuunl)f'r ol 

^■ach econiorfih tv|)e are uresciil ftn must ishuids. ont; 
niij?;ht pr(;dlrl that econioiph types have c\(jl\ed more 
than once within ishin<!s. The phylogeny, hoAve\er, 
r('\"eals this not to be lh<' case. Most eeonioiplis ha\e 


Annals of the 

Missouri Botanical Garden 





: I Wj 







FlgLin' 1 . lslan{l-l)}-isLin».l fxainiiialion of llir cvoliilinji oC liahihil -prciali/allim in tlic Grcaler Aiitillrs. Aiiolc plixlot^tmy 
from Nicholson el al. (2005): l)raii('li Iniglhs made iiltraniclric using |K'iiali/(Hl likclilujod (Samlcrsoii. 2002). Pcnali/.ed 
likrliliood was intplcnicntcd ttsing tlic program r'is (Saiidrrsoii, 20():ij. 'Uu^ sniootliiiig paratiirlrr was 0.90, and brancli Irngdis 
were scaled lo relati\c llrne by assigrnng llir root noilc an ail)ilrary age — 100. Ml ilcniral and Sondi Vtnerican branches >vore 
subsequenlly |)runcd oul using [\w program TreeKdil (llanibani ^K (diarlcslon. 2001). Tcuninal la\(ni ii;nn<'s were renu)ve<l for 
coneis(aiess, but may be viewed, along uilh ihc hve fih, online at <http://biology4.wusd. ediiAlososlab/<inobs_nibg_2005/>. 
Eeoniorph designation is based on previous analyses or, lor some newK desei-ilx-d species, |-ej>resenls new inlcrjjrctatious 
based on the species' description. In a lew eases (bosos eK lU- Onciro/. 1007; (dor el ab. 200ry), ec{anoijili sjieeies occur on 
nearlj) islands (e.g.. the Irunk-ciiiw n caniliacn.sis group in (aiba also coiilain> (^'oniorphologicallv similar species in the 
Bahamas, bit tie (dayman, %'a\assa, and blorida). hi die figure, these species arc included uilh their (/reater Antilleaii rclali\e: 
I.e.. ;dl cfirolincnsis group s[)eeles are iiidiealed as f'uban truuk-cri»\\ u anob'>). 


Volume 93, Number 1 

Losos et al. 
Caribbean Lizards 















I IruntCroi 




Figure 1. 




only a single 

lime on ail Inland, lliuLi^li 

evitJciue exists for Iwo iiislances of exoliition of t\vi^ 
anri grass-hush aiioles on holh Cuba antl ITispaniola 
(however, a phylogenv in whieh the two hNig lineages 
in (jiha are sister laxa, implying a single origin. Is 
ainiosi as well-su|)porte(l as the phylogenv in Fig. 1). 

In a(l(hli(MU either li-iink-groiincl or grass-hiish anoles 
liave e\(il\(Ml twiee on I'urrlo Kieo (the nested position 
of thi' Irunk'irronnd A/n/Iis miudhiclii Peters, 1876 
\\ithin a elade of grass-husli anoles makes distingnisli- 
ing I)etween the two possil.)ilities ihffieult; set- 
Biandlc) i^- de Queiroz, 2001) and trunk-eroun anoles 


Annals of the 

Missouri Botanical Garden 



crowti giant 

1. garmani Stcjiicgcr, \W^) \ui\y ha\t; 

]itay lia\r ('\()l\('(l Iwicr on Jamaica (all('niall\ (4) llic [\\c paradox of eccmiorpli cvolLitioii: repoatrJ cxolulioii 

across isUinds. l)ul f(^\\ inslaiices of TmillijtU' cNoliihoii 
williin an island. Thus, it woidd ajjpear thai once an 
ccoinoipli c\"ol\e^ on an island, it afhic\cs cc<>Ioj^icaI 

evoh(Ml lr(Mn an anccstia! Ii'inik-crow ri anoic). 

Ecnmnrphs nro grnci'allx not pli\ lo^rnrt u-alU ncslrr! 
within (itlici" ccoriinrphs. \\ illi (rw cxct^plions (e.g.. tlic 
grass-l)U^]i annlc. A/idHs niiJuoIciiis (lope. ]l]()'2. wliitli 
arose Iroiu u illiiti a cladc of Cnban ! funk -ground 
anolcs I Mg. I { and the two other eases tnenlioned 
aliove). niosl eeomoipli ela(h^s are rnonopli\ Ictie and 



MU'V and pi'r\'cnts other lineages lanu entering 
thai niclie. The inahihly (tl inlrockiced species lo 
hecoin<^ nn^asive v\ hen (*(:oh)gieal ly snnihu' sj)ecies 

do not gi\'e ris*' to other eeonioiphs. The "'uni(]ue'' 
hahitat spccialisls also rare]}', il ever, arise hoin within 


occur in an area, in contrasl to ihcij' 

ni\ asneiiess in ai'cas lacki 

h ^ 

ng suen specu^s. niriiier 


a clade of one of ihe eeoniorphs (I'ig. 1; one pos>ihlf su|ij>orts this j)re(h'clion (hosos et ah, lW*?j. 

execjition is ainniguons: two 

i>]janiolan unicjae 

anoles. A. <'u^t'!i('<:;r(th{im} Sch^vartz. 1 978 and A. 

cliristopliei W ilhains, I9()(). form a elad<' with iheetadt^ 
oi Hispaniolan (■i"o\\ n-giants: in turn, ihe sisirr laxon to 
this elade is (lie Piiotio Riean (aviwn-giant 1. curicri 
Merrein, ir»2()). 

lu'oiiiorph and "uni(|ue" hakiital s|)rriahsl clades are 

old. I'Aainmalion of f-iunre 1 indieat<'s thai almost all 

eeoaiorjih ehales arose in the lirst hall of anole 
evolutiouar\ lii>tor\ on nio>t islands (the execption is 
Jatnaiea, the short hraiiehes (j1 which ^ll[)p<)rt sugges- 
tions that Jamaiea was underwater unlil well into the 
Miocene; hnt sec I ledgf\s, 200 I). \\\\\ Iuhs old do(^s that 
make them in ahsolnte terms? \ er\ (tid. aeeordiiii' to 
several lines ofexnlcnce. First, \i one aoco[)ts clock- 
like e\(>lution ol the mtD^N A r(^gion cxaii lined, tlie 
niaxiniuni jiairwisi- ihKiM'iMK^e among species cxcctMls 
40% (after correction for niiilt iple suhslitnlKnis). 
which suggesis e\olutionarv di>^ei'';cnee more than 
30 million years ago (i)ased on ealihralion from Macey 
el al., I99[j). Sceoruk mierocoin|)lenient fixation, an 
ind(^[)endrnt molc(ailar ch")ck eslitnation hased on 
dl\ei"geiie(! in alhninin prot ( a ns. pr(»\ ides a \e\y 
similar esliinate tor the earliest fli\('ru(Miee within 
Anolis, H5-10 niillioii \ears (Sliodial <X Dessaiier. 
19ol). Third, three fossil amhtr anoles from thi' 
Dcuninican Kepulilic date to tlie iMiocene or pos^il)lv 
ohha- (Rir'ppel. MXJO; de Queiro/ ct al., 1098; Poleyn 
et ilk, 2002). Two of these speeiniens are whoh' 
animals (ihe tliiriL deserihed hy Pole\u el ah (2002) 

than the heaih and 

The a(ht{ttive radialitxi scenario liingcs on the 
assuni|>tion ihat anoh's inleraet stiongly. IikKhmI, 
a wealth of data (re\ iewed in Losos, 1991; Itongh- 
garch'ii, 1995; more recent examples inchide Leal et 

ah. 1998; Loses & S[)iller. 1999; Cainph(dl. 2(K)()) 
attests lo the strenglh of int(M"specific interaclions 


r I 1 


among anoie species, i nese studies come ni a \aiiet) 
of forms. in(du(ling experimental nuudpidalions. 
naluial ex[)erimenls, and c(ni][)aiative ec()h)gy. StiuL 
ies (htcumeiil effects in tfains of (fifferences in giouth 
rates, hahitat use, reprodnctixc rates, and density. 
Despite ihe great vai lelv of study s) stems and 
apju'oaclies taken, one result is rea(hly appartMit: 


tend to interact stroii'il\ . 

symp)alric anole speed cs 

Re\ ie\\ of these studies leads to se\eral coiudusions 

(Losos, 1991j: lirst, the more sinnlar specdes are 

ec(dogically, the stronger ar<' the interaclions hetween 
them: second- anoh^ spe<a<'s all<M" their hahilat use in 
iht^ presence,^ of eca)]ogically similar species: and. 
lliinh anoles evoLe [d"ienoly|)icall} in response to 
shifts in hahitat use. 


e(nn[)ris(^s lilllc more 

inurphonieti icalt}' Iiutistinguishahle 

f r( ) m 



aimlcs, indicating that at least one 
eeomorpn ciadc was present > 20 millinn \i-ars airo 
(de Quclrcf/ rl al.. 199r,). i\lure(^\ cr. the liinik-(a()>vn 
ain)les fro til I lisfianiola, the ( hi()r<)c)a!nis group, 
comprise an ancient (Tuk^ (Lig- I )- '■.\^\^\ tlie amh(a" 
specinuais cannol he osltMtloiiicailv disl ini^mslied from 
t^xlanl menihers (tf ihis group. 

The {^xohitionary (Ji\ergence and stasis of ecomorpli 

t\ pes can reasonahl\ he luteipieted as the r(^su]| ol 
inlerspecilic interactions. These interactions, howev- 
er, also luue like!) phued a role in within-ecomftrph 

When exannidng diversit} williin ecomor|)h cdath^s, 

several |)atlerns are appaixait. First, many s[)e<.des are 

allopatfically or })ampati"ically distrihiitcd. At least 

some of these allopalric forms ai'c hjcaled in dillerent 

mountain ranges. '\\w most parsimonious explanation 

of these distrihutioiis is that the)" reflect the earl\ 

stages o( allopalric spcciation: po[)ulations thai have 

TIh^ (dassic modtd of a(hiptive radial ion posits thai hecoiiH^ isolalfnl and diverged to ihe point that they 

ecological interaclions, pi-imarily intcrspceifu- com- ar(^ likely to l.)e reproduelixxdy isuhiled. \\\ this 

|)elilion, drive ecological divergence and adaplalion lo context, llu^ use hy anoles of their dewlap (ati 

different parts of ihi' enviromnenl (Simpson, 1953; exiensihie flap of skin located on [lie throat; Lig. 2) 

in comniniiicat KMi is fort inloiis. S\ inpatric anole 
liowev er. would he ihe [)re(liction that (nice one sperdes in\ ariahlv difh'r in some aspect of dev\ hip 
sp<Hdes spe(daliz(^s for a parlicniar asp^n-l of the 'Mesign'' (color, patt(aii, size); these differences 
envii'onment, oilier lineages should have dirncully ap|>ear tft he used as s])eeies recogniliou signals 
occupying this niche. This prediclion could explain (revi(nve(l in Fleishman, 2(1(10; Losos, 2001). As 

liii; Hoi.t: ot' FcoroeicAi, Imiji \ctio\s ix l)i;i\i\(i 

VxiH.t: Dl\ KlisU IC \TI()X 

Schluter, 2000). A corollary of this hvpothesis, 
lowev ei\ would he ihe [)re(liction that (nice one 

Volume 93, Number 1 

Losos at al. 
Caribbean Lizards 


2. Dewlap diversity in Caribhean anoles. — a. AnoILs allogas (Bai-l)OLir & Ramsden, 1919), Cuha 
(Ganiiati, 1888), Jamaica. — c. A. uicslre'i, Cuba. 


b. A. grab ami 

a result, it is possible to icleiilify allopatrically to be ecologically very similar; that is, they are 
distributed taxa that are Iikel\ lo l)e reproduetively ecoh)gically equivalent, bul occur In different places. 

isolated in a non-arbitrary way. 

Of course, because the ranges of these species are 

Many of tliese allojiatricahy and parapalrically often small and in out-of-lhe-way places, the ecology 

distribuled taxa (which correspond to the concept of of many of these species is poorly known, so 
"allospecies" or "semi-species'"; Mayr, 1963) appear slalemenl must l)e considered tentative. 



Annals of the 

Missouri Botanical Garden 

Not all ol lliese species are ecological]) similar, incnihcrs of the same ecomorph class, wliicli partition 

resoiii'ces along axes other lliaii tlie strnctinal liabilal 

ho\ve\"er. Tii some cases closely related species liave 

differentiated to adapt to local conditions. For axis (which is the axis that is partitioned between 

example, m^'mbcrs of the Anulls cyboles Cope, 1862 econiorphs). An alternative possibility, of course, is 

group in Mispamola ar'e ada[)!ed lo use a vaiiely of ihal tlie differences pertnilling coexistence arise after 

different liabilal types, such as puie forest, rocky synipalr) (ihe classic model of characler displace- 

terrains, and semi-deserts (Clor et ah. 2003). ment). Although detailt^l examination of pai'ticnlar 

cases is required lo (hstingui.->h these two scenarios. 

Moreo\'(M*, these ecological differences avc so great 

as to pei'Miil sympatry in some cases, the exlreme of the existence of ecological divergence in allospecies 
whi(di is tin- Irimk-gronnd anoles of Soroa, in western indicates tliat sympatry is not recpiirtMl to drive 
Cuba, wh(M"c (ouf nipmlxu's o( the sagrei grcuip coexist. 

di\ crgcncc. 

I)} a combination of their thermal and WlTlllN-Sri-cil-^s DlVKHca-A'cr: 

All four of these species can be distinguishetl 


struclural mit;rohabitats (one species occurs in hot, 

open habilals at the forest edg{% a second in rtdalively 

open areas widiiii the forest, and tW'O in (lee|) forest; 

the latler two. in turn, fhlfei- in their use (if bouhlers the mid-1990s on several Lesser ATitillean anole 

within th(^ forest, with one species, .4. mesirci IJaibour species revealed higli levels of inlcr-pojuilalional 

& Kamsden, 1916, always toufid on or near boulders genetic iJllTerentialion in mitochondrial DNA (Mal- 

or rock walls; bosos et ab, 2003; see also Rnibal, hotra & Thorpe, 1991; dliorpe & Malhotra, 1996; 


Kecrenl studies have added an unexpected new' twist 
to the scenario detailed above. Studies l^cglnning in 


e geiHM-ally, a pattern exists in me ecoiogi 


Schneider, 1996). Although a number of sn])species 
ical bad |)re\dously \wcn described for some of tliese 

means b) which closely-relaicd members tjf the same species (as many as 12 U)V Anolis marifioralus Dumeril 
ecomorph type are able to coexist. In the ecomorphs & Ribnm, 1837 on Cuad(doupe; Lazell, |072j, levels 
that occair on or near the ground, the trunk-gi'onnd and 

of genetic differentiation exceednig 9% uncorrected 

grass-bush ecomorphs, sympalric species usually sequence divergence between geographic haplotype 
differ in lh(M'mal microhabilats, as just discussed for clades w^erc unexpected, particularly for densely 

Soroa (sympatry of grass-busli anoles in eastern Cuba po|)ulal(Hl, mobile organisms such as 
requires further study; at this point, ec()h)gical anoh^s. 


differences are not known, but few data arc available). 

Further research, however, reveals llial the same 

extremely liigh levels of 

By contrast, sympatry in the more arboreal ecomori^h pattern is found in (Greater Anlillean (Jacl^man et ab, 

types (Irunk-crown and crown-giant) is eorndatcd with 2002; Clor et ab. 2003, 2004; Kolbe et ab. 2004) and 

(hKerenees in body size, which correlates with prey Amazonian anoles ((dor et ab, 2001). Ongoing 

size (nTcHMices in Losos, 1 994). Thus, sympatric research indicates tlial 

tiunk-grtnind and grass-busli anoles tend to be geogra|)hic chffe rent iai ion in mitochondrial DXA 

approximately the same size, but occur in different may be the norm (R. (ihtr, unpublished), 
microtdimatcs, whereas sympalric trunk-crown, twig. These results are exciting for several reasons. First, 

and crown-giant anoles tend lo be more similar in 
microhabilat, but differ in body size. 


and most generally, they indicate that, despite 
40 years of intensive work on anole evolutionary 
These patterns of ecological divergence in mcml.)ers ecology, one aspect of anole divtasitv has been 
of an ecomorph class lead to the following scenario: overlooked. Second, the results suggest the existence 

first, sp(a-iatioii occurs in allopalry. The mechanisms of unrecognized evolutionary units, perha|)s w^ortliy of 
contributing to allopatric speciation watbin islands are 

recognition as specH\s. As a result, un 




poorly und<M-slood, but one recent study suggests that diversity of anoles may, possibly, be much greater 

than j)reviously recognized. Of cours(\ robust dl- 

Ilut:tuating sea levels and tectonic events have 
contributed to [)o[>ulatioii fragmentation and allopatric 

agnoses of morphologicall}' cryptic species wi 


at a laudear locus in one Cuban group su|)ports the 

di\ergeiu:(! in Cuban trunk-crown anoles (Clor et ab, require more than mitochondrial DNA data (Moritz, 

2004). Most allopatric populations remain ecological- 1 99 !■; Sites & Crandall, 1997). Analyses of variation 
ly similar (llie ronc(^pt o( "uIcIk^ conservatism"; Webb 

et ab, 2002). This ecological similarity pixxludes major intraspecific differentiation identified by 

sympatiT wdien allopatric species come into contact, mtUNA (Clor et ab, 200 1), but tlie same is not true 

b.^ading in some cases to para])atry. Second, in some of at least one Lesser Aiitillean species wliere the 

instances, allospecies diverge to adapt to their local pattern of gene flow inferred from microsatellite data 

environments. Third, such divergence someUmes 
permits syuipatry, leading to the coexistence of 

disagrees with that of nilDNA (Stenson rt ab, 2002). 
Further work examimng other loci is n(^cessary to lest 

Volume 93, Number 1 

Losos et al. 
Caribbean Lizards 


the liypothesis iIkiI these forms are genetically 

Non<^tlieless, when iliese closely related species — 
which occii[>y the same structural habitat niche and 

If these forms are geneticall} (Hstinct, then what are are members of the same ecomorph class — are found 
currently recognized as single, island-wide species in sympatrieally, ihey do partition resources. Whether 
the Greater Antilles may, in fad, be complexes of the (hffcrcnces among tlicse species arise prior to 

sympatry and are a necessar}^ prerequisite for co- 
existence, or whether they arise after sympatn^ in the 

parapatrically-distributcd species. Such parapatiy 
w^ould suggest that the (onus are ecoloiiically identical 

and thus unable to coexist in sympatiy. Certainly, same sort of character displacement process pre- 

gg,^ sumably responsible; for ecological divergence be- 

ecological dilferenccs had iiot 


Iv b 

identified for most of these populations, so the ^^^^en the ccomorplis, is not yet clear. 

hypothesis is reasonable, though requiriug further, 
detailed invest illation. Nonetheless, to ihe extent that 

Regardless, these closely related sympatric species 
indicate that adaptive radiation has occurred within, 

is the result oi the same sort of evolutionarv ecological 

the liyi)olhesis is coiTect, ihen ihese recent findings on ^» ''^^^^ ^^ between, econioipli classes. At least some, 
intraspecific differentialion extend the scenario for l>nt certain]) not all, of the diversity withni econiori)hs 

differentiation pr(>[)osed above for semispecies: the 

r ^ . ■ i-rr r r in it* r processes responsible, at a deeper phvloeenetic level, 

iirst step ni (lillerentiatK")n may be the evolutu>n ol i t ' t i . & ' 

for evolution of th<' ecomorphs themselves. 

A second message to be taken from the anole stoiy 
is diat adaptive radiations often must be studied at 
multiple levels: at the level of clades, species, and 
po|)ulations. Only by stu(l)ing all of these levels can 
we get the most complete picture of the patterns and 
processes responsible for evolutionan^ diversification 

in Caribbean anoles. 

ecologically similar forms that occur in alio- or 
parapatrv: evidence of these forms comes not ouly 
from allopatrically distril)utcd populations recognized 
as different species, but also by the existence of 
genetically differentiated populations that are para- 
patrically-distributed and may be reproductively 


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Baldwin. B. G. 1997. Adaptive radiation of the Hawaiian 

silversword alliaiiee: Congruenec; and conflict of phyloge- 
lu-lic evidence from inulecular and uon-niolecular inves- 
ligalions. Vp, 103—128 in T. J. Givnish & K. Sytsma 
(edilors). Molecular Evolution and Adaptive Radiation. 
Cambridge Univ. Press, Cambridge. 
Brandley, M. C. & K. de Queiroz. 2004. Phylogcny, 
.^comorphol<.)gIcal exoliilion, and historical biogeograph) 

Evolutionary diversification of Anolis lizards in the 
Greater Antilles c:onfornis to our ideas about adaptive 
radiation. On each island, species have diversified, 
producing a set of species adapted to different 
ecological niches. Studies on extani species indicate 
that sympatric species routinely experience strong 
ecological interactions, the strength of which is 
a function of how similar ecologicall) two species 
are. Moreover, species alter their resource use in the 
{presence of ecologically similar congeners and, over 
evolutionarv time, evohc ada|)tatious to their altered 
regime of resource use. In sum, the evidence for 
ecological interactions as [he dri\ ing force in adaptive 
radiation is probably as strong for Caribbean anoles as 

it is for any other grouj). 

However, this is not the wdiole story for the 
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species are ecologically similar, but not sympatric. 
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speciation [>rocess of these species (at least ecological 
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sympatric species; sec Losos, 2004). Moreover, some 
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Know ille. 

Creer, D. A., K. dc Qnciruz, T. R. Jacknian, J. B. Losos & A. 
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de Queiroz, K., L,-R. Cliu & J. B. Loses. 1998. A second 
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Dieckniann. U, & M. Doeheli. 1999. On the origin of species 
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Elslrutl, J. ^Sl D. J. Irschick. 2004. Fvolulionaiy coirelations 
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adapt to tlu^ particular environment in which they 
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evolution of anr)linc lizard dewlaji color. Pp. 209—236 in Y. 
Espmark. T. Amundsen & O. Rosenq\'ist (editors), Animal 
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Annals of the 

Missouri Botanical Garden 

C\oi\ n. F.. L. J. \ ill iX A. Laixfu. 200 1. A niuleculai 

ph\ !()<j,(MH'lic aiial\'sis of (!i\ ci'sification in 
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I. J. Ki)ll)(\ l\. Powell, A. Lai'SfHi iK' J. H. I.osos. 

i\ l()j2^(MK"tic analysis of ecologica 

and ninrpliolo^- 
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liiiihal, R. P-JOl . Thermal I'elalionsof li\ e sjiceics of Irnpicnl 

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Thorpf^ Vx. S. & A. iVlalholra. IWO. Mol(^cular 

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Trans. Rov. Soc. Pondon 3oP 815— o22. 


Verheyen. F.. W. Sal/ljLir<iri\ .1. Snocks & A. Meyer. 2003. 

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Vietoria, EasI Africa. Science 300: 325-320. 
Wehb, C. ()., D. D. A(kerly, M. A. VIcPeek & M. J. 

Dono<j:hue. 2002. I*[i\ logenie^ and communit\ ecology. 

Annual Re\. Eeol. Sysl. 33: 475-505. 

Webb, J. K. & R. Shine. 1094. F(M'(hn- liabils 
and reproilucLi\"e biolo^ry of Australian pygojiodid 




f the genus Apnisla. Copeia ]99d; 390— 

\\ illiams. E. E. 19*2. Ilie oiijiin of faunas. f',\ohition of 
lizard con^u'cners in a complex island fauna: A tiial 
analysis. E\(j1. Biol. 6: 47-f>9. 

. 1983. Ecomorpbs, faunas, island >'v/x\ and diverse 

end points in island radialioiis of 1/?o//.s\ Pp. 326-370 in 
R. B. Huey, E. R. Pianka & \. W . Sclioener (editors), 
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Univ. Press, CamJjri^.l're. 


J.orcu H. Rieseheri^~ 


H) 1)11(1 sprcialion refrrs to ihc cslahlishiiii'iit of n(>\rl lubiii! grii()[}jK\s tlial arc rcprodLictixely isolated (loin lludr panaital 
species and genetically stabilized. Most fVequenlls. ii-prodiietive isolation is achieved via an increase in jiloidy. Ho\\e\er, in 
some iiislant:es new hyhiid s])eeies arise and become reproducli\'e!v isolal(M! widiont a ebang(^ in chromosome nimiliei-. 
a process known as diploid or ''lioaiupluiir Inhiid spcciation. The annual snnflowfis of llie genns llt'luinlluis providf^ a well- 
studied c\aiiij)lc oJ this laller mode of speciation. \ \c\\\ I re\ iew llii^ work, placing indi\ uhial sliulie^ in their propei" eonlcxl. 
These inr-ludc (1) computer sinmlations that deserihe the e\ f)lntiouar\ condilious imder which hyhiid speciation is most likel); 
(2) rnole(ailar phylogenetic studies that documcul llie origins of three hvhrid sunflower species; ('^) cotnparalive genetic 
matJping studies that describe the kar\ot)pic c'hanges associated with lubricl speciation; (4) exp(;rifnenlnl re-ci'ealions of 
honiopluid h}hrid specit's that allow genotyple and plieuot\pic comparisons hctweiMi syutiielic and ancient h\hrid lineages; 
(5) qiianliLiti\(' I rail locus (QTI .) stuihes that desci ibe the genet ii- basis ol plienut} jjIc diflcrciices between the parental ^>peclcs 
and the mode of gene aetiori underlying the gtMieralion of (^xtieme j^henotvpes in hybrids; (6) ph\ higcogi-aphic stndi(\K that 
estimate tlie ages and munjier of origins of (^ach hybrid species: (7 1 sch-ctiou studies that measure die slreuglh of selection on 
iiidi\iLlual trails and QTLs in s\ iithctic h\l)rids transplanted into h\brid habitats; and (8) candidate gene stu(hes that >carch loi- 
correlations bct\veeii candidate genes for ecological di\ergence and traits and QTLs .-,hou n to be under selection In the habitats 
ol the h\brid species. Ongoing work includes searches for the mohuadar signature of selection during hybrid spcelallon, 
snrA'cys of gene expression shilts associated with h\brid speciation. and ex[]erlmenls thai evaluate the roie of new hybrid <];(Mie 

eouibinaticjus versus reproducli\e isolation in the ecological divergence of h>bi"i<l 

Key uoids: t'cological di\eigciice, genelic mapping. HtAiinilJius. honmploii 


i\ brid speciation. OTT,s. reprodm-lbe 

from hvhrid /ones. whi(di allows fit livhiid ^retK- 

to tlie reproductive isolation of the hyhriilizintr 

Species oft(Mi roiiie into contact hefoi't* re[»rofhicli\ e 

harriers are fully fornieih resuhing in the formation of conihinatious to Ix-conie estahlislied (Buerkle et ah. 

hybrid swarms or h}"hrid /ones. The eonsecpienees of 2()i)i)j. Although seemingly rare, ibese stahili/ed 

hybridization are most ffe(piently discussed in relation hybrid lineages are much easier to detect and sttidy. 

As a consequence^ much of whal we know about llie 

lineages. That is, the hybrid zones ma) l)e staljle, role of hybridization in adaptixe e\(thilion comes from 

reflecting a I)alance between dispersal and selection the studv of these Ii\brid races or species (Rieseherg 

(Barton & Hewitt, 1985). Alternatively, lh(-y may be el al., 2003). 

ephem(M-ab due cither to the strengihcnlng of re- Finally, a significani component of die lilcraltn'e 

productive barriers and cessation of hybridizatioii on hybridization and its consequences has focused 

(Noor, 1999) or lo the weakening of repioduclive on the means by wdiicdi these new hybrid lineages 

become reproductnely isolated from their parental 

el al., 2001). All ol thi-se consequences are well s[)eeies. Most comtnonly, isohilion arises as a bv- 
documented empirically, although their frequencies 
remain poorly tniderslood. 

barrn^rs and fusion of \\\c hvbridizin"; liti(MU(^s (W olf 

The consequences (t[ |]\ bridizalion ma\' also Ix 

prothict of hybi id genome duplication or allopolyploi- 
dy (Stebbins, 1950). However, reproductive Ist)lati(ni 
sometimes develops \vithout a c]iang(^ in chromosome 

discussed \vith respect to adaptive evohiiion (Ander- numb<M'. a mode of speciation called diploid or 
son, 1919; Arnold. 1997). bi stable li_\hrid zones, for honu^ploid Inbrid speciation (Grant. 1981). 

example, favorable alleles will move ra[)idl} across 

\u this paper, I j'cvicu a series of studies conducted 

hybrid zones, and thereby contribute to ada[ilalion in by my lab oxei' llu^ past 15 years that describe die 

the recipient species. This ''ada[)tive trait introgies- origins of three diploid hybrid sunflo\ver species, the 

sion" may be comnn)n. but It is dilTIcult to detect means h\ which th(n ])ecame reproductivelv is(dated 

because the introgressing alleles will spread rapidly from their panmtal sjiecies, and th(^ lb(n)ry undei-lying 

to fixation and are unlikely lo be "cauglit in the act'' the process. This narrative serves sc\eral |)urj)oscs. 

(Barton, 2001). Less Ire(pieutly, hybrids may escape l-^irsl, our theoretical and empirical work provide 

'The autlioi-",- research on lionioi.)luId h\brld speriatlon ha> been supportetl b_\ the I .S. National Seieiiee l\juiidalIoii and 
the National Institutes of H(\dlh. 

■" Depai tiiient of BIoIoua. Indiana L niversltv, R!ooniin<>:ton, Indiana 17105, L .S.A. 

Ann. Missouri Bot. Gaud. 93: 31-48. Published on 31 May 2006. 

Volume 93, Number 1 

Hybrid Speciation 


convincing evidence that hybridization can contril)ute which monitored the consequence of hyhti(h/ation 

to adaptive evolution 

and suggest that it 


between species thai (hflcred in karyotype (McCarthy 

sometimes serve as a mechanism for large and rapid et ah, 1995). There were two possible outcomes — the 
evolutionary transitions. Second, the work illustrates 

generation of a stable hybrid zone or the origin of 
a novel hybrid genotype Uial (hsplaced die parental 

the kinds of experiments required to rigorously assess 

hybridization's role in evolution. Finall}, the sunllow- species. The latter outcome was considered hybrid 

er hybrid speciation story is currently scattered across speciation, but it probably is moie correctly viewed as 

the hterature, appearing in more than 25 papers. This the merger of species through ]iybri(nzation. In most 

narrative ties these pieces together, placing indi\i(hial documented hybrid species, the parental species 

studies in their proper context. 

Hybrid Speciatiox: Thfoiiy 

continue to coexist with the derived hybrid (Riese- 
berg, 1997). Thus, our group developed a computer 
simulation model to investigate the conditions for this 
more conventional kind of hybrid speciation (Buerkle 
Hybrid speciation refers to the process in which et ah, 2000), which is the focus of this [)aper. Our 
novel genotvpes generated by hybridization become model was similar to tliat of McCarthy el al. (1995) in 
isolated from their parental species and other hybrid its inclusion of chromosomal rearrangements, but 
genotvpes and become genetically stahilizinl. Re- differed by providing a novel habitat in which hybrids 
productive isolation is straightfonvard for hybrids with were favored, as well as the possibility of spalial 
increased ploidy because hybrids between polyploids sepai'ation between die novel hybrid habitat and that 
and their diploid parents typically have an odd of the parental species. 

number of genomes and may therefore be largely 

Three possible outcomes were {jossible in our 

sterile (Grant, 1981). In contrast, homoploid hybrid model: hybrid zone stasis, hybrid speciation. and 
speciation represents a 

challenge to evolutionary 
theoiy, because homoploid hybrid lineages must 

adaptive trait introgression, in wliich one of the 
parental species colonizes the novel liabital by 

become established despite the possibility of back- acquiring advantageous alh'les from the other parent. 

crossing with their parental species (Turelli et al.. This latter outcome was by far the most common. 


Three mechanisms have been proposed by which 

Hybrid speciation was less frequent, l)ut il (hd occur 
at a significant rate ^vhen the sterilily barrier isohiting 

a homoploid hybrid may become reproductively the parental species w^as weak and hybrid genotypes 
isolated from its parental species. First, the new were strongly favored in novel, open habitat 


hybrid lineage may diverge kanotypically from its strong ecological selection). In contrast, hybrid zone 
parental species through the sorting of chromosomal stasis ^vas rare, apparently because of the presence 
rearrangements that differentiate the parental species of novel habitat in which hybrid genotypes had 

a fitness advantage. 

(Stebbins, 1957; Grant, 1981), and/or by the estab- 
lishment of new chromosomal rearrangements induced fhe conditions required for (he indcpcnflcnt 
bv recombination (Rieseberg et al.. 1995b). Second, it evolution of the new- hybrid species following its 
has been speculated that hybrid founrler events may origin are surprisingly different from those favoring 
facilitate hvbrid speciation by pro\ iding initial spatial establishment in [ho lirst place (Buerkle et al., 2000). 
isolation for the new hybrid lineage (Charlesworth. Although a weak sterility barrier between tlw paren- 

1995). Third, a hvbrid lineage may colonize a new tal species favors speciation, it also translates into an 
habitat or niche and thus become ecologically isolated 

even v\c 

aker barrier between the new hvbrid liiK^age 

and its parents. As a consequence, the genetic 

nvw hybrid lineage cannot be 

f tl 


from its parental species (Grant, 198 1 ). Hyl)rid 

species often occupy habitats that are ver)^ different integrity o 

from those occupied l.>y their parental species (Riese- maintained in parapatry with parental populations. 

berg. 1997; ^\'ang et al., 2001; Gross & Rieseberg, Thus, for hybrid lineages to evolve independ(Mitly 

2005). This is probably because a novel hybrid from paraj)atric parental jxipulations, the initial sle- 

lineage is more likely to survive if it experiences little rilit) ])arrier between the parental species must be 

competition with its parental species and if di- strong, a requirement that gi'catl 


s tl 

v rccRices me in\cn- 

vergence in habitat preference results in some spatial hood of this mode oi speciation. Ahernali\cly, 
isolation with the parental species (Templeton, 1981; 
Charlesworth, 1995). 

Three simulation studies have examined the pro- 
cess of homoploid hybrid speciation (McCarthy et al., predictions that liybrid speciation is most likely 
1995; Buerkle el ah, 2000, 2003). The first of these following hybrid founder e\ents. in wliich a few 
was a spatially explicit individual-based simidation, hybrids found a new population that is ecologirally 

isolation of the liybrid ncospecies can be maintained 
by strong ecological selection and/or spatial isolation, 
a result that accords well with earlier verbal 


Annals of the 

Missouri Botanical Garden 

and spatially isolated from ilie panMUal species anij}li[ude and facilitating range expansion. In sonic 

(Charleswoilli. 1995; fiies(^berg. 1997). 

instances, hyhridi/alioii was believed lo have conlrili- 

The third sitnulalion study (Buerlvh' ct ah, 2003) iiIimI lo the foi'inalioii ol inlrogressive races (/7. anauus 

was an cxlciisiun of Buerkle el al. (2000), except that suhsp. (exanus Hciser in Texas (Ileiscr, 195 1 h) and 

the novelliahilat for hybrids was eliminated, the sizes //. holnndcri siihsp. hohiuderi in (-ahfotriia (IhMs*^-, 

of the ]i}hi'i(h/ing parental popnlations wi-vid allowed 1919)) or new species (//. negleclus lleiser (Heis(M' et 

to \ary, and the extent of spatial isolation was ah. 1969)). 

rednced. 'I'his new model allowed us to assess the My laboratory re-examined the^c hypotheses usln^ 

relative hxHpu^ney ot the four most im[>orlanl outcomes a combination of moleenlar matl 

of hybri(h"7alion: hybrid /one stasis, hybrid spi^'iation, moh^'ular ph\logcnetic analyses (Dorado et ah, 

adapli\(' trail Introgression. atid extinction of one of 1992; Rieseberg ct ah. 1988, 1990a, b, 1991a. b: 


<(']' surveys an{ 

the parental species (t\picall\ the rare on*^). Hybrid liiesfdxM-g. 1991). We verified much of lleiser's work. 

including the occurrence of nalui'al hybridizati 


zone stasis was most common, occurring In 81% of 

simulations. Kxlinetion ol the rarer sjjecies occurred between IleliatJlInis innuins and each of the species 

only when the sterility bari'itM- was weak and was h>tcd above (Dorado et ah, 1992; Itieseberg et al., 

essentiall) always the n^sult of adapli\e trait in- 1988, 1990a. I). 1998), as well as the introgressive 

trogression. Hybrid s])ecialion occurred iti only 2.1% origin of//, (iimuns subsj). ttwdiins (Rieseberg et ah, 

of the simulations and was faxored by a weak sl(^rilily 199()b). On tin- other hand, the molecular e\idctice 

barrier betw^een the parental species and moderate lo failed lo support a hybrid origin (or //. iwgleclits oi" //. 

strong ecoh)gieal stdcclion. However, hybi'id specia- hohindcri subsp. bulandcri (Rieseberg et al., 1988). 

lion was almost al\va\s accompanied by exiiiictlon of Thus, while the morphological criteria employed by 

one ol the partMital species. These results iudicale that Hciser acc-uratcly identified conlemporary hy1)rid 

the presence^ of novel habitat greatK facilitates Inbrid swarms or zones, their nlililv in ihe (leteclit>n of 


leen snggesieo ny numerous 

ancient, stabilized hybrid lineages was limiled. This 

specialiou, as has 1 

students of hybrid speciatiou over ihe [>ast century was not unexpceleih as it has long I)een recognized 

(e.g., Keruer, 1894-1895; Grant, 1981; Tem|)letoiu dial iTiorpholoi^ical intermediacy mav sometimes 

1981; Ai-nold, 1997; Rieseberg, 1997). Also, without result from pi'occ^sses other than h\ bridi/ation (Colt- 

an open nielu:, one of l!ie |)arental species Is rcjplaced lieb. 1972). 
bv the hvbnd, and total species diversilv remains 


Ill addition to verifying or refuting putali\"e 
examples ol h) biid luieage foniialion, molecular 
All three sinmlatious studies have oik^ remarkable ])h} logenetic analyses detected unsuspected hybrid 
n^sult in common. W Ikmi h\brid speciation does origins of three sijeeies (Fig. 1): JlcliuiUhus anonudus 
happen, it occurs (.[ulckly, often in fewer than fift) \\\Akv. JL desi'i'liroh} I l<'lser, and //. /J^//Y/r/o.v//.v Heiser 
generations. Thus, McCarthy et ah (1995) referred lo (I!ieseberg et ah, 1990b, 1991a; Rieseberg, 1991). 
homoploid hybrid spc^-iation as a punctuated mode The three hybrids ap[)ear Lo be derived h-om the same 
o( specialiou, in which long periods of hybrid zone parental species, //. annuus and //, peliohnis. 
stasis are followed by abrupt transitions In which a However, there are subtle dlf(crenc(\s In tlie pareulal 
new (it hybrid genot_\pe bei-omes estabh>hed. chloroplast and unclear ribosomaJ D\A haplolvpes 

found in each hybrid, suggesting that each was 
Independently dei'ived (Rieseberg, 1991; Rieseberg 
et ah, 1991ci). Over the past decade w(' have exploipMl 
this replicateth naiuial hybrid sj)eciation exptM'imcJil, 
The role of hvbridizatiou in the diversification of in combination wilh theoretical studies, to derive 
North AnuMican sunllowtM's [llelidnlhus L.) was a more pre(hclive theorv of hybi'id speciation. This 
initially c\})lored by Charles Heiser and his students body of wtulv is described below, 
(lleis^n-, 1947, 1949, 1951a, b; lleiser el ah, 1969). 
Heiser documented the occurrence of nattual hybrids 
between the \v idespj'eaih connnon sunflower. H. 
annints T., and several of ils comieners. inchidimr //. 

HvRRII)l/\riOX AXDTHK R\ 01 A"ri<tXA]n hbSTOtt^ 

Natui^ai. His'roin 

The three h\binl species and llieir parents arc self- 
argophylliis Torr. & A. Cray (Heiser, 1951a), H. Inc()mpalible. insect-pollinated ammals, with th(! 
bokuiden A. Gray (Heiser, 1949), //. drhilis Nutt. sattie chromosonK^ tuuiil)er (n = 1 7). All five spin^ies 
(Heiser, 1951b), and //, pctiolaris Null. (Heiser, are native to the continental United States. Tlu: Iwo 

paienlal species have widespread and broadlv oxcv- 
anuiius to acquire favorable alleles from tiie locally Ia|«i>ing distributions that are ccuUnx'd in the U.S. 
adapted sptxdcs, thereby Increasing its ecological Great Plains (big. 2). They differ In soil pr(Terences, 

1947). This liybri(lizati(»n. Heiser argued, allowed //. 

Volume 93, Number 1 

Hybrid Speciation 


perennial Helianthus 
H. niveus subsp. niveus 


100 1 2 




H. praecox 

H. debilis 

H. niveus subsp. tephrodes 

K niveus subsp. canescens 

H. neglectus 

K petiolaris ^ ^ 

^ ^ '^ ^ ^*H. anomalus (sand dune) 
">Cj>H. deserticola (desert floor) 

H. paradoxus (salt marsh) 

H, annuus 


H, argophyllus 

H. bo lander i 

H. exilis 

Figure 1. Pliylogenetic tree for JJelianihas seel. JJcUanllms based oti eouibiiied ehloroplasi DNA and nuclear i-il)os()mal 
D\A data (redrawn from Rieseberg, 1991, fig. 9). Tlie nuiiilxM- of niLiLaLioiis are given above and bootstrap percentages 
below eaeb branch. Dashed lines indicate parentage of homoploid li)i)rid species. 

however, with Helianthus aiinuus largely reslricled to ihey co-occur, Little Sahara Recreation Area in 

heavy, clay soils, and H. petiolaris to dry, sandy soils Central Utah. 

(Fig. 3). Nonetheless, these two habitats are often Wild sunflower species produce an indehiscent 

fonnd in close proximity in the central and w(^stern one-seeded fruil called an achene (or cypsela). 

United Stales, resulting in the production of numerous Although tlie achenes are eaten by small mammals 

hybi'id swarms and hybrid zones. The hybrid zones are and f)irds, dispei'sal by way of the animal feces seems 

narrow, often less than 30 m, and little evidence of unlikely because most seeds are likely to be digested, 

inlrogression is found outside of the hybrid zones, II seems more likely that sunflowers are dispersed b\ 

apparently due to the synergistic action of several large mammals such as bison. Wild sunflower achenes 

reproductive barriers (Rieseberg et al., 1995a, 19991); are covered with small hairs that can bind to fm', and 


Schvvarzbacli et al., 2(.)0T). 

sunflower aclienes have been reported in buffalo fur 

llie three bylnid species are much more linuled in (Aseh, 1993). There also are reports from early settlers 

eographic distribution than their parents (Fig. 2), of an association Ijetween bison and sunflowers. For 

with restrictjon o[ Ilelianthus deserticola to the Great example, in 1839 journalist Matthew Field descril)ed 
Basin Desert in Nevada, Utah, and northern Arizona, 

bow ''among the sunflower beds the huge back of 

H. anomalus to a handful of sand dune habitats in a buffalo here and there was seen, as the ponderous 
Utah and northern Arizona, and H. paradoxus to salnie brtite Ijrokc down llie stalks l:)efore him while pressing 
wetlands in western Texas and New Mexico (Fig. 3). toward a fresher pasture ground" (cited in Asch, 1993: 

Despite proximity to parental populations, no natural 
hybrids have been i-eported between the three ancient 


In addition to their role in dispersal, the distur- 
hybrid species and Uieir parents. In contrast, the three bance generated by bison may have created opj^ortu- 

nities for hybridization. Hybridization has long been 

hybrid species are almost completely allopatric to 

each other, but 1 have observed hybrids between H. known to be associated with natural and anthropo- 

anomalus and H. deserticola at the only site where 

genlc (listurbanee (Andei'son, 1948), and, as shown by 


Annals of the 

Missouri Botanical Garden 

□ Helianthus annuus 
EH Helianthus anomalus 

S Helianthus deserticoia 
H Helianthus paradoxus 
Helianthus petiolaris 

CiMt^ia|)liic ilislrilmlioiis of ilx^ two pamiUil sprcirs and tlicii- ijii-fv livhrid (lrri\ ati\ c sjircies 

Figurt' 2. 




o assess uio rule ol ^ciioiuk- restiLuUinii^ in 

the following passage from Bar>M(^ss (1985: i), the T 

impact ol hisoii on (he Great Plains was profound: hyJ)rid speelation, we liave generated detailed genelle 

""IIk^ [hison] herds marked thc^r [(a-ritoiy with trails, linkage maps for the llu-ee liyhrid speeies, Ilclidnllnis 

thousands o( ilietn. some shallow traees, some eiglit- anomahis, II. dcseiiicola. and 11. pdradoxus, as widl as 

to-ten-ineh tRMKdies, others so deep that the animaPs ihcir pulati\e parental speeies, //. annuus and //. 

sides would rnh the embankments." Iverieeting either 


or eoineidenee, mierosattdlite divergence 

places the origin of the thr(;e hyhrid Hcluuiihus 
speeies betweiMi 63,000 and 2 1 (),()()() general ions 

petiolaris (liieseherg et ah. 1993, 19951): I ngerer et 

ah, 1998; I5inke et ah, 2002; Kieseherg et ah. 2003). 

These ma[»s wej'e (leve]{)])ed using a eomhinalion of 
AKLP, HAIM), anfl SSR (microsatcllite) markers, with 

ago (Scdiwar/haeh & Puese])(^rg, 2002; Welch ^K more than 650 markers jdaceil 
Rieseberg, 2002b; Gn)ss et al.. 2003). or jus! ahcr Aliirnmenl of 

on e 






the colonization of North A 

/vnKM'ica l)v 


son ca. 

200,000 >ear> ago (Darv, 1971). 

(MindiogoLis markers across the five 
maps alldwrd ns to rectjnsti net the chromosnmal 

rearrang<'mi'nts thai liave a(H'om|>anie(l hybrid speci- 
al ion. 

Kar^'ot^ ric Kvorr'rioN 

All tl 

li\bri(ls hs 

ne(' iiNOruis nave nrider<'(Mi(^ massiM' kar\-o- 

tv]-)ic re-organi/ation. Ncjt onl\ (hx^s each of the hybrid 
speeies possess a uni(jue combination of parental 
(diromosomal rearrangements, Iml also a minimum of 

As discussed carHer, lheor\ indicates that the 
develo[)ment of reproductive isoIatio!i between the 
newhyl)ri(l Inu^iges and their [jarental species ma) be three, two. and five chromosomal breakages (and an 
lacibtated bv rapid karyotypic ev(»hition (Grant. 1981; equal ntnnber of fusions) luv nniuired to achieve the 
McCarthy et ah, 1995; Buerkh^ c\ ah, 2000, 2003). IMianllnis (in<>malus^ H. (Irsrrlicula. imd fl. parado.xus 

genomes. r(^specti\ely (Rieselierg (M ah, 19951), 2003; 

Most verbal and simulation models luuc assumed thai 

the karyotypic change occurs through tlie sorting of Burke el ah, 2004; Lai el ah. 2005). We hi 

a\ ( 

preexisting chromosomal rearrangement.- that differ- previously shown that approxlmatelv 50% of the 

eiUiate the paretilal species (Stebl)ins, 1957; Grant. reproductive harrier l)etween llcliaiillnis sp(x-ies is 

1958). However. Templeton (1981) noted thai re- caused by chromosomal rearrani-ctnculs (Rieseberii et 

combiuation in hybrids might h^ad to additi(.nal ab, 1999b). Purthermore, crossabilitv and inUM-fertilitv 

diromosomal hirakage. sludif.-, (Ric^cluTg. 2000. uiipuhlislicd) indicale tlie 

Volume 93, Number 1 

Hybrid Speciation 


Figure :\. Plu.tograplis of llic Iwo parciilal species aiul llieir three hybrid derivative species in typical lialjitats. 
Pliotographs by Jason Ivlck. 

three hybrid species are slrongly isolated from eaeh 
olher and from their paixmtal s[)ceies (Fig. 4). Thus, as 
predicted by theory. ra[)i(l karyoly[)ie evolution in the 


Inhere is a rich literature describing the recovery of 

hybrid sunflower species appears to have 

facllllatcd lertility in synthetic hybrid lineages and the degree of 

the development of repn.duclive isohition widi d.cir their isolation from theh" parental species (Slebbins, 
parental species (Templeton, 1981; Buerkh- ct al, 1957; Grant, 1966a, b, 1981). These early studies 

were important because they demonstrated that 


Annals of the 

Missouri Botanical Garden 


a n n u ii s 





I'i^Lii'i' 4. (.nts.sal>ilitv ;mkI iiitnfeilllitv ainntin llir l\y( 



^l(.'rIvaU\c s|)cclcs. PcrciMila^cs imlicatc [tollcii \iahilil\ of first irfriciatioii 
rr])n>(ln(li\c (orniialibilil} . 

parciilal si^ccios, syiilliclic ll^ln■i(l liiieao^cs, and ilm-.v \\\\nn\ 

i_\l)ricls. lliicktirss is propoiliimal lo 

lioniopltnil liyl)ri(l s|>ec-iali()n was (easiljlc. Ilouever, feasible. l)iil llial il potential!) 

they (lid not atlempt to replicate naluraliy oeeurnng ra])i(lly (Un^erer et ah, 199Si). In addilion, tl 

hybrid speeies or eonipare the newlv sytilhesized svntlielte hybrid bneai^es were slron-lv isolate(' '' 
livbi-id liii('a^ii,('s \vil]i those alreadx existing in nature. 

(MKud occur \'er\ 



The Hi'lianlhus work fills diis iinpoj-laiit t;-a|) in th( 

their parental species, \vith mean polJcJi ferlilily 
ran^in"- from 29 io 42% for crosses with Hcllai/lliiLs 


anfud/s anri 10 to 13% for erosses uilli //, priiolaris 


We ahctiipled to rephVale the origins of die hvlu-id (Fi«^. 4; Uieseberg, 2000). luanarkably, the ll 
speeies l)y synlhesizing livltrids belvv(u^n the two indeixMidcaitlv i^ejiejated hybrid lifu^a<^es were hi-ihJv 
panaihil s|)ec!es, Ilt'lidnlJins (mnuus and //. pcdnldris.^ itilerhMlile \\hon c-rossed with (^aeli olliei': ineaji pollen 

and subjectin^u ihe syndietic li\biicL~> to selection for 

leililily o\cr several genera!i(»n^ (Rleseberii (4 ah. This result implies that the thn^e h\ brid lineages have 

1996). I?eeansc sunflowtas are self-ineompalibh^ and eon\erg(Hl onto a fairly sinular set of pareulal genes 

eai-|y ^(aieration hybrids are scani-sterile, iiybii 

speeiation in diis giouji 

ferlility ranging bom o3 to o9% (Hiesebejg. 20{)(1). 

or ("hroniosomal sediments, hideed. nuMotie anaUses 


involved both l)ack- indicaled llie s\ iilh(4ie lineaires were sinnh 

n" ni 

crosses aiu 



r I ^ 


ore. we em 


kary^ilvpe, \ar\iuu in onlv oni- 

both k]iid> t)[ erosses, but \ aried the order of li-aii>locations (ivieseberu-. 2000). 
backcross and filial generallons in three independent 

oi two recl[)roe 





o explore I lie genonnc 



le vc 


s were gi-atil\ in<i-. Aher only f 

similariU o( (he svnthclie 
li\brid lineages, we screened ca. (>() individuals from 
our each lin(\ige with 197 UKthnadar maikcrs specific \o 
generalioiis t.f s.dection. pollen fertility in the three one oj the oilier parental species (Rleseberg et ah. 
]i_\brid lineag(\s had incrcas<Ml from 5.6 to 9I.;i%. 1996). Genomic cougru(aice. a< measm-ed by the ([) 
""'i*'^'''".^ '''<" f'"' n-eoveiy (tf hMlility not oidy was eoelficdent (a standard measure of association thai can 

Volume 93, Number 1 

Hybrid Speciation 


vary froni -1 lo 1; Sokal & Rulilf, 1995), raii^i^cd frnm in iiakire (Ungerer et al., lOOo). The latioiiale for our 

0.65 lo 0.75 (/•* < O.OOOI) for comparisons ainoii^ llio nielhod is thai in a newly forming hyhi'id species the 

three hyl)rl(! hneagt.'s, a result thai accords well witli sizes of parental chromosomal segmeiils are ex|)ected to 

the high f(Mlility repoiied for crosses hetween dieses hecome progressively smaller over lime (hie to re- 
lineagcs (I\i('sel)crg, 2000). 




congruence ni genomic composilion 

among the synthelic hyhild lineages, it seenu^l sensi- 

comhinalion (Fisher, 1953; Baird, 1995). However, 
conlimied reduction in segment si/x; will he countered 

hy stahili/ation of the hyhrid sp(M'ies' genome; suh- 
hle to (h'lermine if \hr three natural hyhrid s[)ecies sequent recomhinatiou w 111 he among s(.'gments derived 
had found a similar solution to the prohlem oi li}hiid from the same parental species (Ungerer et ah, 1998). 
sterility. This was a more difficult prohlem dial This anal\sis repres(ait^ an ciujiiiieal api)lication of R. 
required sur\(^ying natural populations of hotli llr- A. Fisher's junctions approach (Fisher. 1953). which 
lianlhns (uinims and //. peliularis to determine the tracks parental species segments l)y monitoring re- 


) pare 

ntal origin o 

f eacl 

1 marker mappe( 


e comhinatiou hreakpoints or "junctions" hetween het- 

three ]i}hrid r^pccic^ (Rieseberg et ah. 1993, 1995h, erogcneous regions rather than all points on a genome. 

2003: Ungerer et ah, 1998). In all, 427. 290. and 325 fn a neutral case, we can imagine a "junctions clock," 
of the markers ma[)ped in //. auonialus, II. (Icscrficold, 

which is analogous to the molecuilai' (dock, I)Ut slows 

4 4 

and //. paradoxus, respectively, c(mld he assign(Ml to over time as heterozygosit)- decreases due to di'ift. By 
one or the otluM- parental species and dnis were comparing the frequency spectrum of ohsi^rved parental 

species' chromosomal segnienis with predictions hased 

on comj)uter simulations (Ungerer el ah, i99[>), it is 

the tluiH^ syndictic ])ossihle to estimate the nuniher of g(Mi(M-ations retjuired 

to stahih/e the genome of a hybrid species. Note diat 

informal i\c with respect to genomic composition 
(Rieseberg et ah, 2003). Genomic congruence was 

high [oi 

h\ brul 

■ comparisons 



ineages and either 


anonuiiiis or 



w^e are estimating the speed of hyhrid speciation. 

dcscrlicola: ([) ranged from 0.44 to 0.50 {P < 0.0001) 

for comparisons with H. anomalus (Rieseh<Mg. 2()(){)) not the age of die h)brid sp(M-ies. 

and 0.53 to 0.59 (P<0. 

) for comparisons wilh //. 

To date, we haxc onl\ estimated the tempo of 

Jeserlicola (f{iesel)erg. unpublished). In contrast, bttle speciation for one of the hybrid species, llehauthus 

aiionialiis (Ungerer et al.. 1998). This s[)(;cies has the 
largest number of mapi^ed species-specilic markers, 
tliereby allowing the most precise empirical estimates 
of chromosomal segm(Mit lengths (Ungerer et al., 

contrrnetK:e was ol)served hetween th(^ three svnthelic 
lineages and //. paradoxus: 0.28 to 0.34 [P < 0.01 
Akso, note diat levels of genomic congruence accord 

dationshins (Fig. d^); the 

closely wilh crossing re 



synthetic hybrids are most eom[)atihh' and most 1998). It seems bkely that ihe hybrid species will 

interferlile with H. anomalus and H. dcscrllcola as aiise in hybrid founder popuhitions lliat are spatially 

predicted b)' genomic congruence, but l(^ast com|)al- and/or ecologically isolated from the i)areulal species, 

ihle and least intcrfertile with H. paradoxus. From Therefore, we modeled this scenario by simulating 

a broader [)erspective, these resulls in(hcale thai a liybrid swarm, starling uilh e(|ual numbers of//. 


\ sc 



um piays a major roic ui (icu-rmnung 



annuus and //. pcliolaris iinhx iduals, and ahowing 
hvbrid genoiule composition and that the number of recoml)inalion to take ils course in small, closed 



oris o 

f didereut >i/es and under different 

solutions to the problem of liybrid sterility may he 

fairly limilcd. Clearly, H. paradoxus has found selection regimes. Th(^ sj)(U'd of hybrid speciation was 

a difh^-ent solution than the other taxa. Possibly, diere estimated by comparing the sizes of chr(nnosomal 

were differeul j>roporlions of the parental s[)ecies in the segments in the simulation studies with those ol //. 

hybrid /on(^ from which FL paradoxus was h)U!i(l<'d and/ anomalus. Chromosomal segment sizes in the H. 
or the genomic composition of //. paradoxus was 

anonuilus genome were large, STiggestIng 

that its 

strondv infhienct^d bv ec"olo*iical selection (F(^\er et 


nome became stabilized in 10 to 60 generations. 

ah, 2()03a, b; Hieseberg et ah, : 


s re 

Trmpo ()!■ IUmkii) Speciatto\ 

suit accords well with earlier simulation 
studies of hybrid speciation in which new^ hybrid 
species typically became eslahbshed in ca. 50 
generations (McCarthy el ah, 1995; Buerkle et ah, 
Botli tlieoretlcal and experimental studies of liomo- 2000) and argues that the tempo of homoploid hybrid 
ploid hybrid speciation indicate that it is likely to occur speciation, like aUopidyjdoidy, is very rapid, 
veiy I'apidly (Stebbins, 1957: Grant, 1966a. b: Riese- 
berg et ah, 1006; McCarthy et ah, 1995: Buerkle el ah. PiiK\(rrYPic DiM-:K(;K.Nr,r 

2000), but until rec(Midy no methods have been 

available to test I his prediction. We have devised 

a mclhod for estimating the tempo of hybrid special ion 

The ihree hybrid species inhabit what are argual.>ly 
the most extreme habits of anv sunflower (dune, desert 


Annals of the 

Missouri Botanical Garden 

Tcil)l<! 1. Hypollu-tical cxaniplc oi li'ansgrcssivc segregation due lo ihe eoniplenienlary action oT geiies willi addllive 
f^ffeels (d'om Rieseherg el al., 2()().'5). 




I'iicnotyplc \alue:^ 

Species A (AA genol\|)c) .Species B (H15 genoly[>e) 

+ 1 

+ 1 
+ 1 


+ 1 


+ ! 
+ 1 

Ti-ansgressivc I'^ 



Transgiessive I 2 



eaeii o 

r ii 

lloftf, atid salt marsh hahilals; Kig. 3) and have eoiidueUMl in tlie iialural hal)ilals of 
diverged sigjiificantl\ from die parental species foj- parental species (Lexer el ah, 200;?a: Gross et ah, 

2004; hu (hvig et ah, 2001). Thus, transgre^sive 
segregalion. which is connnonly ohserved in segre- 

man}- traits associated with diese hahitats (Sehwar/ 
baeh el al, 2001; Roseiitlial et al.. 2002). A 


[)rovideri a simple nieclianism ioj' die ecological 
divergence o( h\hrid lincaiies. 

Cr.NETics or TiiANSCRKssiM. St:t.;nKf;ATi()N 

importani question Is wlielher hyhridi/alion enuld gating hvhtid popuhilions (RieselxMg- el ah, 1900a), 
provide the [)h(Miol)pic variation necessary f(jr 
colonization ol these hahitats. 

\^ e adfhessed this question hy eompai*ing plieno- 

typie variation in die du'ee ancitaU hvhrid species, 

synthi'tic hybrids (a RC2 population of lldianthus 

afuuuis X H. pclioldfis)^ and Ijoth parental species 

grown in a eonnnon greenhouse environnuMil (Ro- 

sendial el ah, 2002; Rieseberg el ah, 2()();5). A total of 

Ide history, and ecophvsiologieal 
trails were measured. 

40 moiphologicah 

So how are extreme pIuMiolypes generated in h\hrid 
populalions? \innerotis possibilities have been sug- 
gested (deVicente & Tanlvsley. 1903; liieseberg el ah. 
1999a), iufdnding an elinaled mutation rate, reduced 
developmcaital stability. nnn-additi\ c effects of alleles 

As ex[)ected, gi\('n their divergent habilat ]n-efer- al (he same (o\ erdoiuiiiance) or (hilerent (ej)islasis) 


unmasking of rare reeessi\e alleles, and the 

ences, ihe ancient hybrid sp(M'ies (hffered signifieaul- 1 

ly from the parenlal species (or many of ihe measured cotnbitialion of alleles with effects in the same 

trails: 20 for llcliantlius anonidJus (8 intermediate, 12 (hrection Crom both parenlal speei(^s (complemenlary 

extreme), 14 foi" //. dcscrlicold (4 intermediate, 10 geiK^ action; Table 1). 

We enij)loyed quantitative trait locus (QTb) 

methods to determine the 



of gene action 

extreme), and 2d. (or //. paradoxus (8 inUM'mediate, 16 
extreme), bitermediale traits are easily accotmled for 
b} hybridlzallon because ihe entire plienotypic 
continuum between the parental species is found in 
segregating hybrids (({iesebcrg el ah, 200.'5). 

11) hridi/ation t-onld account (or most of the extreme section was genotvped (oi- 96 molecular markers, and 
traits as well. Indeed, for 28 of the 40 traits, RC2 1 u3 Qdd^s were detected for the 40 traits. Remarkably, 

underlying Iransgressive segregalion in Heliaruhus 
(Rieseberg et ah, 2()(«). Rriefly, the same I5C2 
populatit)!! em[)loyed for |)henolyping In tlie previous 

plants had phenot\[nc values that 


39% of the OTLs had effects in the oj)posile direction 

exceeded those of the parenlal sp(Mdes, a phenomenon of species dilfcrences and 34 of 40 trails had at least 

known as transgressive scgr(*gallon (Grant, 1975). one opposing (YYL. That is, for diese QTLs, the H. 

Overall. 10 of 12(83.3%), 10 of 10 (100%). and 11 of annuus alhde prodticed a more H. prtiolans-Wki^ 

16 (68.8%) extreme traits in llclianlhus anomalus, H. phenotype, whereas the //, petiolaiis allele produced 

deserlicola, and H. paradoxus, respect iv(dy, were a phenot\pe ihat was in die direction of H, anuuiis. 

within the range of the BCo popuhitiou. The handful ddiis is exacllv the kind of genetic archileclure ihal is 



conuucue lor lransgn^ssi\ e segregation undej- the 

of li'ail \alues exceeding those in the RC2 population 

might have been Iransgressive in a recqnocal back- complemenlary gene action model. 1 1\ brid indnddiials 

cross population or have arisen through mutatiotxtl that combine all of the "plus" or all of the ''mitms" 

divergence rathi'r llian hybridization. In tdtluM" case, it OTLs f 


roni Dolli parents for a given trail will have 

is (dt^ir thai the majority of extreme traits observed in Iransgressive phenot)i)(\s (Table 1). Although com- 
th(^ ancient hybrid species could have l)een gtaierated plementary <y^e\w acdion explained most of the trans- 
through hybridizalion. These results have now been 
re(>licaled bv similai 


gressue [iluMiotypes, epi static niteractions were 


' common garaen (^xjXM-iments 

detected for 18 trails as well, 'bliese results 

s are 

Volume 93, Number 1 

Hybrid Speciation 


similar In those obtained for cultivalecl plants; (Hieseberg et al., 2003). That is, we asked ulietlier 
coniplenienlaiy gene action is most freqnenl, but the hybrid species had the predicted set of QTL 
epistasis and ov(M-doniinance do sometimes contril)ute adeles for producing their phenolypes. If hybri(h/a- 
(deVicente & Tanksley, 1993; Rieseberg et ah, lion played a key role in phenotypic divergence, then 
1999a). a significant correlation should be found between 

[)rc(licled and actual genomic composition. 

Genomic composition of the ancient hybrid species 

(hd accord closely with predictions from Hie QTL 

analyses (Rieseberg et ah, 2003: Fig. 2). The c|) 

- T50; 

GEM-rric Goiun:i,ATi()NS 

Transgressive segregation via <:'omplementary gene 

action pro\-ides a m(vms by which extreme phenotypes coefficient of association ranges from 0.56 (A' - 
may be gentM-aled fcjr individual traits. For a hybrid F < 0.001) for Helianthas paradoxus, to 0.58 {N 

193: P < 0.001) for IL anomalus, to 0.65 (/V 


lineage to successfully colonize a new habitat, 
however, all of the trait differences must be combined P < 0.001) for 77. deserticola (Rieseberg el ah, 2003). 
into a single individual or genotype, which may be Thus, liybridizaiion does appear to he largely re- 
difficult because of linkage and/or pleiotropy for sponsible for the phenotypic divergence of the three 
QTFs underlving key traits. Thus, genetic correlations hybrid species, 
mav limit ecological divergence through hybridization. 


To determine the role of genetic correlations in the 

Karlier in this paper, I reviewed ca idence suggesl- 

selection plays a major role In 

ing that fertility 

ecological divergence of the hybrid sunflow^er species, shaping hybrid genomic composition (Rieseberg et ah, 
we asked whether closely linked or pleiolropic QTLs 1996), whereas the QTL comparisons (h'scribcd above 

suggest that phenotypic (presumably ecological) 

in the 15C2 population described above have eflects 
that are in the same direction with respect to the sehn-tion must be important as well (Rieseberg et 
hybrid species phenotype (Rieseberg et ah, 2003). ah, 2003). What is the relative importances of these 
These positive correlations w^ould greatly facilitate two modes of selection? A preliminary comparison of 
ecological divergence and hvbrid speciation. 

We found closely linked QTLs were indeed 

le two data sets indicates that in many instances 
diere is concordance betw^een the predicted genomic 

positively correlated in direction of effect (Rieseberg composition from fertility selection and the QTL 
et aL, 2003: Fig. 1). The (J) coefficient of association analysis of phenot>pic differences, perhaps implving 

overlap between hybrid incompatibility genes and 
256: P < those responsible for phenotypic differences. Also, the 

ranged from 0.32 (/V = 256; P < 0.001) for 

Heliaruhus paradoxus, to 0.47 [N — 

0.001) for IL aaomalus, to 0.53 (.'V = 256; P < combin(^d data set more completely accounts for 

0.001) for //. deserticola. Thus genetic correlations hybrid genomic composition than either individual 


lata set does alone (Rieseberg. unpublished). 

likely facilitated rather than impeded the origins of 

the three species, particularly for//, anomalus and //. 

deserticola. 1 lowever, our results also imply that PnM.()C;F,()(;iiAlMlY 

geiuslic correlations may limit the number of ecolog- 

icallv relevant midti-lrait phenotypes, perha[)s ex- Comi>arisons of the genomic composition of tlie 

plaining why only three new^ hybrid species have ancient hybrid species with synthetic hybrid! ineages 

and predictions from QTL studies (above) suggest that 
homoploid hybrid speciation may be repeatable. Hius, 
we asked whether the ancient hybrid species had 
arisen multi[)le times In nature. This was accom- 

originated from this cross. 

lIvBRii) Si'Kcii'.s' Gi:n()mic Composition and 
Predictei^ Pm-:No-rviM:s 

f tl 

pHshed by surveying natural po[Hdations oi tiie 
parental species and their three hybrid derivali\"es 
that most of the phenotypic differences associated for variation at chloroplast DNA and nuclear micro- 

Allhoudi studies of synthetic hvbrids demonstrate 

with each of the liybrid species could have arisen 

satellile loci (Schwarzbach & Rieseberg. 2002; W elcl 

through hybridization, they fail to prove that this is <S. i^ieseberg, 2002b; Gross et aL, 2003). ^'e also 

what actually happened. It could be, for example, that 
the differences arose as a consequence of mutatiijual 
divergence and that hybridization was incidental to 
phenotypic evolution. To distinguish between these 

assessed crossahility and interfertility among j)o}tula- 
tlons oi Uelianthus auouicdus and //. deserticola. In H, 
aiiofiudus, the crossing studies were complemented by 
meiotic analvses of inter-populational hybrids to 

two hypotheses, we compared tlie genomic composi- determltie the chromosomal basis of variation in 
tion of the three ancient hybrid species with 


For a singh' origin, all populations of a given hybrid 

predictions from the QTL analyses of the BC2 

population of Uelianthus anniuis X H. petiolaris species are expected to have the same chloroplast 


Annals of the 

Missouri Botanical Garden 

DXA luip]()ty|)(', lo form a tiioiiophylelic liiuvigr hasrcl of 16 rxtrctne traits in H. paradoxus coiiiu be 

on unclear niicrosalcllite loci, and lo he highly repiiealeil in synlhelic hyhrids, implying thai the 

inlerlcrlllc (i.e., ha\'e a single kar)-oh'p(^) when creation of th(^ H. paradoxus pheno[\ pe may he a rare 

crossed. For midtiph- origins, dillerent popnlations c\ent. A similar paltern was ol)scr\ed foi' genetic 
A a sj)ccies may vary in chloi()[)lasl DNA haj)lotvj)(^ 


correlalifins. Tii'hllv linked (jrLs mostly had effects 

and the s[)ecies is unlikely lo he monoph)letic with in the same dirtx-tion \\ ilh respecMo tlu^ pheiioL) pes of 
respect [o nuclear micrusalelhte loci. Also, significant ihe apparentlx nuihipl) derived //. annnuiJus (4) ^ 
variation in ha'lilily fhie lo kaiTotyplc \arial)ility is 0.47) and //. dcscrficnla (c|) = 0.33). hi contiast, 
pre(h(i(-d for intcr-|)Opuhili()nal crosses. Note Uiat genetic correlations make il difficnh to r(-creale llie 

= 0.;52), 

nudliple chloropla^t D\A haph)lypes and [)olyphyly mulli-lrait plicnot\pe of //. paradoxus {(\) 

fnr nuclear mici-osale!lite loci can also result from 
a single origin lolloucd hv iulroa:ressio!i with t)[ie or 

which appears to have arisen onlv once. 

l)oth [larental species. However, suhstautial \ariation 
i]i iiit(M--|)opulati()iial crossahililv and interhHliiity or 
karyolype is uidikel\ in this hitler scenario (Sch\var/- 

bach iX Rieseher^i. 1^002). 

R(:()ix)(;i(:\L Sl■,l,l■.CT]{)^ 


Iheorelical studies in(hcate ihal slrt)ni!: ecolo'iical 
selectior! is a prere(]uisile (or successful Inhrid 

lohxtnlar and crossahilil}/lulerrertihly evidence speciation (McCarlh) el ah, 1993: IJuerkle el ah, 

2000). Also, our studies of phenol\pic dirferentiation 

siiggcsl at least thi-cc diflercaii origins for llcliaulhus 

anonuilus (Schwar/hach & Itleseherg. 2002). Tlut have assunuHl that 

ecological stdeclion is the 


ileiK nil: force (hi\ in<i diver'^ence. IIo\vever. il ma\ he 


dial some of the j)hciiol\'j)ic dilhM-cnccs result from 

species has thi-ee main chioroiilasl DW haplotvpes, 

one appaj-(nill\ deri\cd from //. aiinuus and the other 

two h-om H. prilolaris, hikewis<^ [\w species has three neutral processes or ari^ a hyprodiicl of selection on 

fertility grou])s thai arc complclelv corrclale<l with [lie correlated traits. Correlaled selfM-lion is liktdv lo he 

|)articularl\ imj)orlanl in h\hrid speciatioa, l)eeause 
the unit of seleclittn is the chromosomal segiiient 

Ivvo rct-iprocal translocations, as wouhl he |)redicled rather llian individual gene or nuilallon. 

for mulli[)le origins. However, there was no apparent 

signatmc of multiple origins in the nnch^u' micro- 

salellile dala. perhaps due to gene flow among ihc 

distrlhulion of chloroplast DMA haplot\pes. Meiotlc 
anal}-ses indicate llie lertility gron|)s differ h\ one or 

We ha\'e employed hotli comparative and (experi- 
mental a|)|)roaches to identify traits liked y lo liave 
been under s(d(H-Lion during hyhiid sj)eeialion. The 
comparative approach locuses on Irails in the h)l)rid 
spc^cies thai are common lo other taxa sharing its 
liahitat. For example, ll 

le saiH 

iwine endemic. 


independently derived iiiuvtgcs snl)sec|nenl to hybrid 

I*altcrns ui molecular \aiiation in Hcllaiulius 
desrrlicola were also mosi cousistenl ullli multiple //c//a/;/////.w//?o/;;a/u.y, has many trails associated u ith 
orignis (Cross ct ah, 2003). The s|)ecies displayed four (hme habilals such as very laim-. cyhiidrical scmmIs 
(h(T<arnl chl()roj)last D\A haplotypes (one imm fL rai)id early root groutli. and succulent leaves 
annuus and three hom //. pctiolaris), pol\|)hvlv al 
microsalellile loci. au<] considerable niter-j>opulation- 

iei(^ was 

al crossahililv and interfertilitv. Tl 
con;iru<'iice between the three data sets 


(Schwar/bach et ah. 2001: Rosenthal el ah. 2()02j. 
Large seeds iwc thought to represent an adaptation for 
burial avoidatice, wl 

wiuM'eas a round or cyiuKUic 



niakitig it more dilfn-nlt to rule out llie ])ossihilil\ of 

shape may pie\-ent seeds from being blown i\\\i\\ from 

tlu^ d 

)y ni- 

a single hybrid sp(M-iatio!i (went followed I 
Irogression with |)opulali(t[iN of the parcnlal s|)t;cies 

H^ (Uine habitat. Large sc(nls aLo 


\Kv\\ con 

tribute lo 

rapid early root groulli, whici 



<'onlrast to Uclianilius ajwmahrs and //. 

1 enables seedlings lo lap 
inio watr'r fvscrves dcciKM- in the sand dunes. Finally. 
sncculcnl lea\es may sei-\(' to reduce water loss and 

anrasion dy 




o\\ mg sand (Dauin, 1 99t; b 



desert icola^ H. paradoxus i.-. dei'i\ed from a single 

hybrid s[)eciatiou event (\^VIcli & Hieseberg. 2002bj. 

All surveyed popnlalio!is of llu^ sp(M-ies share a single 

chlui-oplast I).\A haplot)])(^ (derived from //. a/niuus) reduced 

and (orm a single clade with 99.8% bootstrap support (Kosenthal v[ ah. 2002). The lirsl two traits ensure 

1996). fleliaullnis deserlicohi has man} of the c 
h'alures of a desert annnah ifudnchng rapid riowcring. 

height at mattn•it^. and small, narro\\ lea\es 

basf^d on 1 i microsattdlile loci. 

ra|)i(l reprctdnction f 


on owing neavy seasonal ram, 

The apparent numbers of origins of the three hybrid wh(M-eas small narrow leaves decrease water loss and 
species corndales welt uilh ihc results b-oiii Uie a\ oid fatal overheating (Chapin (U ah. 1 987; Cihson, 
morphological and QTL analvses. Ten of 12 extreme ]998j. fh'llaulhus paradoxus shares several traits with 

or haloph) Lie speides, including 

other sall-lo\ ing 

traits in llchanlhus anonudus and all 10 extreme trails 

in //. descrlicola could hi) i-e-t-rcaU.'d h\ li\bridi/ing increased leaf succulenc(wmd an efficient meciianism 

populations of tlu^ par(aital species. How(n(M-, only 1 1 for reducing mineral ion uptake (Welch & Ries(d)en>', 

Volume 93, Number 1 


Hybrid Speciation 


2()()2a; T.exer el al., 20031)). Both reduci- the loxic observalion ihat QTT.s uiKlerlying hoth mineral ioti 

eH\a:ls of sodiLiin and other mineral iotis. 

ujjtako traits and survivorship in the sah marsh had 

Onr experimental slu(hes involved ihe Iransphuila- elfeets in o[)pnsing direelioiis (Lexer et ah. 200.'5a). As 
lion of reciproeal B(^2 synlhelic h)l)ri(ls into the 

discussed earlier, this kind oi genetic arehitectm'e 


hahitats of the (hree ancient hybrid species. We then 

measured the strength of selection on indi\idual traits 

atid (for Helianlhits pantdoxus) the QThs underlying of /I. pdnidoxus might 

them. For//, afiomahis, we focused on hvif eco[)hysi- hy hybrids. 

UTKierlies transgressive segregation and [»ro\ uies 



a simple explanation for liow the salt marsh ]ial)ilat 


* + 

lave Deen original y couju 


ological traits, phenology, and vegetative bioinass, 

The Old. data also allowed us to lest a fundamental 

with fitness estimated as reproducti\e biomass rec[uiremcnt for homoploid li}l)rid speciation. lh)mo- 
(Lu(h\ig et ah. 2001). Although we liad piv(hctcd ploid In hrid speciation rej)reseuts a kind of synn)atric 
tliat selection in the syndielic liyhrids would mostly ])c or ]>arai)atric speciation, and niochds of speciation 
in the direction of the //. anomahis phcnotype, this 
was not necessarily the case. Only for leaf succulence 

with gene How indicate the strength of selection at 
individual loci must be grcalcr than tlie migration rale 

in the BC2ann hybrids (backcrosses toward //. <uuuins) (Maynard Smith, 1966). Tlua-efore, we calculated 
and water use efriciency in the Rf^^P^'l h\brids selection coefficients for mineral ion QTLs in the salt 
(backcrosses toward //. petiolans) was selection marsh hahitat (Lexer et ah, 2003a). The selection 
toward the H. anomalus phenotypc. For mo.-t trails, (-(KdTicients were larger (-0.08 to +0.13) than any 
the direction of selection was depend(Mit on the conceivable migration rate for sunflowers, indicating 

it would have been h^asible ("or IJelituitluis panidoxus 
to arise in sympatry or ])ara|)atry with its paiy^ntal 

genc^tic background, suggesting th(^ existence of 
nudliple adaptive peaks for Heluinllms in the dune 
habitat. Although these results seem inconsistent with 
the multiple origins of the species (Scln\ar/bach & 
l\ies(^berji. 2002), it niav be that feitilitv sehn'tion or 
selection on other correlated traits drive early 
eneraticm hybrids toward just one of these peaks. 
I\esults from I he selection ana])scs in the 
llrlidnlhiis desert icol a environment wia'e ecjually 


CAM)i[)ATr. Ci:m:si-oh EcoLotacAL Di\i-:rgi:.\ce 




arlditioual genomic regKjns associated w nn s 
tolerance^ (f.exer et ah, 200 Ij. The salt tolerance 
candidates were identilied from an expressed se- 
quence^ lag (KST 


for Ilelianthus paradoxjts 


1. On 

binaliy, we have assayed setiiience polymor])hisms 
for sail tolerance (candidate geiu^s in these same l?(;2 

popuhilions to determine w^lu^her any of the candidate 
difTIcult to interi)ret (Gross et ah, 2()(M), Kor two of ^..^^..^ ^^^.^^^ ^^^ q^Ls of inlerest, as well as to identify 
tlie key traits, leaf area and flowering date, selection 
dilferentials and gradifMits diftered in sign in l)oth of 
le BC2 t)opulatlons. Thus, while it is clearb leasible 
for (lir(v*tional selection to produce the H. deserficola 
pheuotv])e for lliese ti'aits, it is not possible to prinlict 
the pheuotvpic outcome of such selection li-om the 
present experimenl. For the third key trait, st(an 
diameter, selection In the synthetic li\brlds was 
consistent, but in the opposite directiou of the //. 
descrlicola phenotypc. ^khis result is puzzling and ma} 
possibly relate to the experimental design. In whi(*h 
seedlings were propagaled at Indiana Uni\('rsity and 
iheii lrans|Kn-ted to Utah for trans[)laiilatIon. In such 
weak and etiolated seedlings, it may be ihat large 
stems would be fa\()red, whereas narrow stems might 

l)as(ul on luttnology to genes witli known iunction. Kfwc 
of the II genes, a Ca-dep<Mident protein kinase 
(CUl*K), maps coincident with a previously identilied 
OTL for mineral ion uptakes Two additional genes (an 
El{-I\|)e calcium ATPase and a transcriptional regu- 
lator) also exhibit a signiricant fitness effect in the 
wil(k or course, these stuihcs are correlational only 
anil f'lUK-tion will ha\e to b(^ vtaified by transgcaiic 
compleuientation or RNAI. Nonetheless, diey indicate 
we soon ina\ be able to examine the role of indi\idual 

be favored in seedlings j)ropagated under natural. 
high liglu conditions. 

Only in lieUatUlius jHiradoxus habitat was the 
direction of select ion in the experimental hyl)rids 
consistently in the direction ol the //. pantdoxus 
pluMiotvpe (Lexer vY ah. 2003b). P(xsltl\e directional 
selection was detected for leaf succidence and Ca 
uptake, two traits that are known to mitigate salt stress 
in plants. In contrast, lln' uj)take of Na and other toxic 
mineral ions was strongly negatively selected in the 
salt marsh habitat. Of p;reater si'inificance was the 


genes in ecological divergt^nce and speciation in 




{)\cv the past 15 years, my lab has studied how new 
h>l)rid hpccles may arise without a change in chromo- 
some number. Our main contributions include: 

(1) Mdteculai- docunieiilalioii of ih*- hyhrui origin of llircc 

(lislinct saiifluuer .s|)ccics from the same pair of 
ftan-ntal sptulcs (Jvicschcrg et ah, 1990h; Ricschrrg, 



Annals of the 

Missouri Botanical Garden 











( 1 1) 

Dtn(*l(t[irncnl nl the fii>l genetic- nijp foi a hmiioploid 
li\l)[i(l sneeies ( I^iesebeiir el al.. \^)^)'.]). 
Demoiislialion lliat li(mi(i|)l(>i(l Ii\ l)i u! ^[K'cialion in 
wild sunt low CIS lias lieen aee<)in[jani(Ml h) rapid 

kar}<)l}|iie evolution as pre(liet<'(l l)\ \ci'l)a1 models 
(liieseherg el al.. IMO.ll); Lai et al.. ^OO.T). 

Fxperl menial ic-c real ion of luunoploid li\ ln'id spe- 

ei<.-s ill sLinflower and demon.shaliim ol genomie 

eoiigriienee of s\nllielie and anei<-nl luhfid s[)eeies 
(ixieseberg el al., I '^96). This deiiioiislrated the 
r(^|)ealal)ihly ol I mm opioid hyhrid sp<-eiatioii and 
I lie niiporlanee ol ferl ilil\ seleetion in shaping In 1 1 rid 
geiiomie eonipo^ilion. 

DemoiistralI(ni of [\\c rapid lempo ol lulnid speeialioii 
hased on the large sizes oTparental ehromosonial hioeks 
in a luhiid siinllowci' speei(\s (IJngvier <-{ al., I W'J). 

C(nn[)uler simulalion ol homoploid hyhrld speciation. 
which verified \ei-l)al dieoi'y atid drmoiisliated die 
e\ olutiunar\ eondi lions Ui\ orahle lo h\ In id ot ijiln 
dillrr from those re(iiiii"ed for the indejjendenl 
e\'oliition of ihe Inhiid sneeies fliiirrklt^ el al.. 2()(l()|. 

, 1 ■, ' / 

l>e-ei"ealion ol phenohpes of hoinoplou 
speeies hv experinu'iilal h\ hridi/.alioii ol eonteni[)o- 
rai) parenla] speeies populations and h"an^gi'essi\e 
segrrgalion [Lexer el ah, 20031); Kieseherg et ah. 
2003: Cross et ah. 20(M.; Rosenthal et ah. 2003). 

Demouslralion thai eoiiinietiienlarN' "'eiic adion is ihe 
piimary cause of liaiisgressive segicgalion in (*xj)er- 
imeiilal sunflower Ii\]iri4ls (Lex(M' el ah, 200.">|); 
Kieseherg el ah, 2003). 

l)iseo\-er} that genetic correlations hieililate rather 
ihan impede the oi'igin of the h\ hrid sinif1t>W(a' 

spt^des (Kieseherg el ah. 2003). 

Demouslralion thai llii^ genomic coiupo^ilion of ihe 
aneieiil h) l.)rid sLuillowcr s[)eeies can hi' predlclcd 
from the OTI, anahsis of phenoh[)ic traits. im|)l\ing 
an important role f(»r eeologieal seh'clion in sha|)in< 
livhiid genotnie eomposiOon (Rieseherg el ah. 20U3). 
IJiseo\er} that t\W) of the li^hrid sundnucr species 
are inultipl} derived in nature as pi-ediclcd from 
earluM' sludies ol the repealahilil} (►f li\hi"id speeia- 
lioii (Selnvarzhach iS. Hieseherg. 2002: W tdeh iX 
Kie.schcrii:. 2002h: Cross et ah. 2003,). 

lifHi when tin- s|)ecies arose iii nature MU)re than 
63,000 years ag;*). Preliiniiiai'v evidence .suu-^esLs we 


iei"(isat(dlile markers 

aiiking the three most 

strongly selecled QTLs in ihe llctianlhns jxinidoxus 
hahitat had si^iiilicanllv red need \ a rial n lily as 
('ompanMJ uilli inicrosatellile h)ei from unselec-ted 
rei^ions. \et I here was no ihllerence in \ a ri ability 
levels hehveen lliese gr()n[)s ol loci in th<' parental 
speeii^s (C. i^dtdist el ah, uiipiihlhshed). 

lexeloped a 3()0()-geiie ahiotic 

Second. m\ 

ah nas (ie\ 




stress niieroarrax for sunflower (Lai et ah. in press). 
We wish to ask whethei- gene expression differences 
are induced hy li}l}ridi/allon and whellicr ihese 
Induced dill<M<Miees conlrihute to ecoh)gical di\ er- 
gence and h\l)iid speciation. 

Thirth we wish to nse the Iivhrid .-^pecit's svsleni to 
address the fundamental question ol whelhfM" adaptixc 
di\ergenc<^ within a species is I i mi led l)y niLitalion or I)y 
gene How from the center ol each spe(des range 
(l\irkpati"i(d\ ^.K Marlon. 1997). dhat is, wh\ did the 

pareiilal s[)ecies nol colonize tlie extreme liahilal^ of 
the ancdcnt h) hrid species":* l*ut another way, was it new 
hybrid gene comhinations oi' repro(]u{dive isolallon that 
alh^ved the h\ hrid specdes to coloinze new habitats? 

FinalK, we will cotiLniue our woik to idenliK and 
characteiize ihe H;enes uikUmK inii (M'oloi!:ical diverirence 

O ,'0 o 

ill this svslcm. dhis wdll in\o]ve a combination (d EST 
s(n|ncn(dng (> 70,0()() KSTs already se(jneiic(-d), 
searclies for genes with the signature of pcjsili\e sclec- 

30 identilied). candichite g(Mie t7iap])ing (close lo 

3( )( ) 


microarrav analyses, and luiKdional 

testing using Iransgenic complciiicnlalion and KNAi. 

Allhough lliis review has focused almost cxcdusive- 
ly on hylnid sniiflower spc(d<^s, there are broader 
issues thai need to be addressed as well. In pailicular, 

(12) Dcmonslration ihat man\ of the traiisgrc^si\e tiaits we need Lo know how fi-e(|ueiillv homoploid hybrid 

disenvered in experimenlal crosses are under selee- speciation occurs in nalure. whi(di will recniiiv b(^tl(^r 

lion ill natural li\hrid liahitals (Lexer cl ah, 200.3a; 
Liidwig cl ah. 200 L Cross et ah. 200 Ij. 
(13) Di-moiLslration thai .-^tdeclion coefficienls for OTLs 

tools lor detecting it in pli}l()g(^netic trees. lAulnnate- 

Iv. help is on llic way. New niellufds of network 


k-rh i 


ecological di\ crgeuce 


paradnxjis are large enough to account for the origin 
of the species in para])atr\ with its [tarculal species 
(Lexer (M ah. 20()3hj. 

tdciilificatiou of several prttiuisiiig candidate g<_'nes 


or (M-o logical (n\ crgeuce in lU'innunus pardno.xus 


(Lexer cl aL. 200 1). 

in Ih'lianlhus rer'onst ruction aie ini(h'r de\eh)pmenl (!-e\ iew(Ml in 

l.inder & Rieseberg, 2001), and the availabilil\ of 
seciuence dala from numerous mndear luetics should 

* O 

pro\ ide far more power i 

histories llian wa.-- possible lu the i)ast. This power 
could 1)0 further <aihaneed if clusters ol linked genes 

or (hdecling rcllcuiate 


Of course, 'here i> nuudi leit lo do. Kre\ ioLisIy, we were se(|uence(h L nder the assumption of li\l)rid 

altempled to replicate the earl\ stages of hybrid 
s[)e{dation by planting segregaling hybrids into ihe 

speciation. separate jjhvlogenelie reconsl ructions of 
individual genes that i 

u'e tiglitly linked should lu 


habilal ol the ancient h)brid sj)ecies and id(MitIf\ iiig the topolog) of old)" one side of the h\l]i idi/alion. 
traits and Q LLs that were under selection. We are fhese recoiistriiclions would be lonolo<iicall\ incon- 

gruiaU with reconstructions h)ased upon cduslcrs of 


cnrreutly extending these ex[>eriments l)y asking 


whetli(n' w(^ can detect the molecular signature of g(aH^s from llie other side of the hybridi/ation. 

selection dui"ing In brid s[>c(dation and il ihe sanu 

We als(» nee( 

lo know whether many of the 
discoveries made in the siniHoNNcr s)sl(Mn can be 
ihc expcriniciilal (lopnhil Ions were also under selec- gen<n-alized to other homoploid lubiid spe<des. How 



al s 

egmciits llial w(a"e under s(declion In 

Volume 93, Number 1 

Hybrid Speciation 


are mosi new hybrid species reprddiietively isolated Donulo. 0.. I., il. Rieseberg & D. Arias. IW2. Chlmophist 

Jroin llielr j)arenlal species? Is ecological divergence 

tli<' iiile rallier tlian die exceplion? Are ihe habitats of 

the new liybrid species typically extreme relative to 

iheii par<aital species, or are lh<'y more accurately 

desci"it)ed as intermediate or recombinanl? \\ hat is 

the genetic Ijasis of the ecological di\ergence in 

lubrids? \\i)\\ repeatahle i> hxlu^ld s])eciation \\\ (itlier 
linc^ages? Are homoph)id Inbrid species oilcn muMi- (^ 
ply derived? What are the charactcrislics o( iaxa (hat 
make them prone to lionio[>l<nil li\ hiid speciation? 

DNA iiilrogressioii in soul ht 'in Cahfoniia siinllowt^rs. 
Evohilinii \(k 366—572. 

FisluM", R. A. 1933. A luiha" theory of jiitichoiis in iiihi'eedinj^. 

IlerrJily H: 187-197. 
Gibson. A. C. 199*1. I^hotoss ritliclic organs <)( dcscrl phnits. 

BioSricncc 18: 911-920/ 
CuHlicb. b. 0. 1972. b{n'eLs of conhdt.aice in [lie analvsis of 

Inbrldi/atioii in jjlants. Aim. Mi.^souii IJol. Card. 59: 

b^ 3-1 16, 

Hopelndy, onr sunflower woi 


vv I 



e an 

e\[)erimental and con('e])tua] gni(b; foi" studies of 
homoph)id hybrid species in other organismal groups. 

LiloraUiro Cilrd 

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Conservalioii Biol. 13: 1039-1033. 



Auji K. Sakai,' Stephen G. Weller,'- Warren L 

Wagner;'' Molly NepokroeJJ, and Theresa M. 



A niulli-disciplinarv tippioacli. infimlii]^ pliylo^ciuTlu analysis, populalloii hiology, and (|iiaiililalive fijenetics. lias helped lo 
cliK'idalf lIk; scIclTIvc faelots lliaE \vd\r [HOiiiolcd spcc-iali(jn and sluds in breeding s\skMns In Scluedca (Caryo[)li) IJaceae). 
Scliicdca is the fillh lar<^est lineat^e in I he nalive I lawaiian flora and the inosi diverse lineage^ w ilh r(^spe('t lo breeding syslenis. 


le ge 

nus is nionophyletie and shares a eoninioti anceslor with a ehide eonsisling of Iwo arctic or boreal-nordi leniperale 
spe<'ies. Most inte't-islatid cnlonizalions were from oldfM' to younger islands, and most ino\etnenl Ijctvveen islands led lo 
snfficieni isolation to resuh in formation of new species thai are single-island endemics rather llian species with multi-island 
ih.-^lribLition.^. Closel) I'elated species j)airs occurring on older islands tend Lo diiler in habitat and arc Isolated eeohigieally on 
llie same Island, wliih' species ])alrs on )(>nnger islands tend to be in similar hal>ital on different Islands. Speciation within this 
lineage has been associated with shifts in habitat, pnllinalion system, and bi'eeding system, including evolution of selling 
(obMgale autogamy, facultative autogamy), nn'xed mating systems, and dimorphism (gynodioecy. subdioeey. and (lioiM-y). 
I)Imoi|)hic breeding syst(-Mis a[)pear to have been dt^-ived indep(Mul(Mitly twice In Schledca, and facultative autogamy and 
obbgate autogamy have both e\olved three linu^s. 'I'lie colonization of windy, <lry liabitats a|)pears to ocfan- before changes in 
sex allocation patterns, and the evolution of dini()rj)hism in this liruvige has been pronioled by the combination ol high 

iubretMiitig depression and high selfing rates. Manv morphological traits associated with allocation lo male and female finietion 
are highU heritable, and geiielie correlations in general do not aj)pear to constrain the e\olulIon ol dimorphism in Scliicdca. 
Key uards: adaptive radiation, autogamy, bi-eetllng systems, Hawaii, Inbreeding de|M"ession, resource al]o<-ation, 
Scliicdcd, selling, sexual diniorphisni. 

bigbest iitcidetice of dioccy of an 

Flo^veriiig plants rcprodnce with a remarkable 
di\ersily of breeding syslenis, even among cdosely 
related species, and the selective forces responsible llora (12%-13%; Sakai et ab. 1993a). 

studied (14.7%), followed tdori(d) by the New i 

y angiosperin flora 



for ibis diversity eonlintie to be of great inferesl. 

Pbyb)genelie studies bave (ducidated lb 

e re 



Ada[)tive radiations in island systems liave been sbips among laxa in some o( tbe larger Hawaiian 
partlcidaily useful bi^ause tbe isolation of remote lineagc^s (e.g., Balduiti et ab, 1991; Baldwin, 2()().'5; 

ar(dupelagos has made ll easier to identify selective 
factors and to discern evolutionary patt(M'ns (e.g., 
Wagner & Funk, 199.3; f/ivnish & S)tsnia, 1997; 

Givnish et al., 1995; Wagncj- & Funk, 1995; Weller et 
a!., 1995; Sakai et ab, 19971); Kim et ab, 1998; 
Ballard tK' S\ Isma, 2000; Balduiti. 2003; Nepokroeff 

Grant, 1998). The Hawaiian Islands bave been of et aL, 2003, 2005; LindcpisI ct ab, 2003; Carlquist et 
particidar interest in the study of plant tiiating systems al., 2003; summary in l^ricc & Warner, 2001). Most 
beeatise of the high incidence of dioecy ni tbe flora. Hawaiian groups lac-k a com])lete }>hylogeny, but 

Worblvvide, the average incidence o 

f di 

(iioecy HI 

because ol tlie great isolation and small size ol tbe 

angiosperm floras is about 4%-6% (Retnier i& native I lawaiian angios[)erm flora (about 1020 
Ritdvbd's, 1995), but tbe Hawaiian Islands have the species; Wagner et ab, 2()05a), it has been possible 

' We thank Amv Duubar-W albs anrl Allen Andres for theii- invaluable iudp in llu' lab and gieetihouse, Denise Mix for htdp 
with the figures, and tlie man} undergraduate researchers in the Sakai-Weller lab at ihe Unberslty of California-Irvine lor 
llicir contributions to studies of selfing rate.^. Inbreeding depression, resource allocation, and quaiitllative genetics. \\^~ also 
thank the National dVopical Hotaiiical Garden loi- logistical support. This work was funded in pari Ity ihe National (ieogi-a[ihic 

Society, National Seienc(* h.undalion (BSH P>('M7616, BSR 89-18;]66, DKB 92-07724. 1) Kb' 98-15878), Smilhsouian 

Scholarly Studies grants. Smithsonian Mellon Fellowships, and tlie Lludergraduale iiesearch Oj)portunlties Proiiram/ 
rifsidential Undergraduate belln\\^.lups of llie L'ni\'ersit) of Califorrna-Tr\ inc. ^^'agner's contribution was eonipleted while he 
was the McBryde Chaii" for Hawaiian Plant Studii\s at the National Tropical Botanical (iarden. 

^' Departnienl of Eeolog) and Evolutionary Hiolog), University of Cali[oinia-Ir\'ine, lrvin(\ (^alilornia 92697, U.S.A. 

H)epartment of Bolanv. MHC-166. Smithsoiunn histilntion, P.O. Box 37012, Washln-ton. D.C. 20013-7012. U.S.A. 

'Biology DeparlnienI, Univ(*rsity of South Dakota, Vermillion, South Dakota 57069, U.S.y\. 

"'Department of Biologic-al Sciences, ML0()6, University of Ciueitniali, (^iiuannati, Ohio 45221-0006, U.S.A. 

Am. MissoLiii BoT. Gako. 93: 49-63. Pubusiiki) on 3i May 2006 


Annals of the 

Missouri Botanical Garden 

lo idciilify plnnl lineages descended (loin a eoinino]! geruMie anal\sis. popidalioii l)i(tl(»ti;y, and qiianlilali\'e 

[he ^(Mielles. to understand holli [he geiielie polenlial lor 

e()l()nr->t and (^\ amine e\nh]li()i]ar\ natlern; 

^^ ni 

Hawaiian Ishnids with r(^speet to sjx'eiatinn (l^-if:e & (lie evolnhoii ()( hreefhng systems in diese species and 

Wagner, 2001), rarity and conser\a[ion stains (Sakai ihe seleeti\(' factors ihal have promoled specialion 
el a1.. 2002). and 1)|-ee(hnt>- sysleins (Sakai rl aL, and shifts in diese lii-ee(hfiii systems, 
lOOoa. ])}. The al)ilit\ to identiK linea'res in the exlanl 


Mora allows examination of Irail^ t-orrelaied with 

l)i'ee(hng sysletTis I ha I c\vr less conrnuiidcd ] 


p1i)logenetic relationships than analyses al the 

d1ie gemrs Schiedea, with 31 sjiei-ies and .'5-') ta_\a, 

species ov e\en the generic le\'el (Sakai et ah, inc hides deci(hHnrs perennials in coastal ha hi tats, 

iy05a; SttMiicr, I9oo). Based on slndies of diese sprawling snitshriihs in mesic foi-esl.s, wood\ shrnhs in 

lineages, dioecious species in llie Hawaiian Ishnids dry, mesic. and uet (oresU rainforest vines, and small 

inc (\c^ccn(\ri\ Ironi dimor[)hic colonists or from snl)al|)ine sul)s1n-nl)s. Scluedcd exhibits thr i!:reatesl 


liermaphnnlitic colonists with \u situ evolnllon (jf di\(!rsit\ in hreediii"; systems of any nati\e Ih 
dioeey in the Hawaiian Islands. Ten perceni of angiosperm genus (Weller et al., 1990; WViler & 
succ(\ssful coloni>ls had ditnorphic hiceding systems Sakai. 1990; WVller el al.. 1993: Sakai el al.. 1997l>: 


and gave iise lo lineages with i nnorphic species. 


iguer el ah, 200r)l)), inelnditn:' I 

g nerma[)liro(lit ic 

These dimorphic Jitieagt^s (with hoth fllmorphic s()eeies thai aic ohligalelv autogamous, facadtalivelv 
colonisis and di'scendenls) account lor over half of 



p;iiii:ill_\ selfitig willi mixcil iiiMliiig 



le (iiniiiipliic spet'ies. l5aktT"s law siiggcsls lliat 




hllicultics ni ohtaining matt 

'S w I 

unit culonl/alion 


systems, as wetl as (Innorpliu* s[)ecies that are 
\nodioecious (fcMiudes and liei'mapln'odites in [■k)[)u- 



y dioecious species more than hermaplncHlilic lalions), suhdioecions (females, males, and a few 
spcH'ies, lull ihe success of diiiioiphic colonists as hciinaphrodiles in popidalions), or dioecious (females 
w(dl as hiogeograplnc patterns widiiii the Hawaiian and males in populations). In this section \\e review- 


laphy, hahitals, and breeding 

Ihc chang<;s \n hH}gcog 

systems thai have oe<airr<Ml dnriu'r diversilicalion of 

tlie lincag(\ Shilts in breeding svslcnis arc associated 

Islands suggest that oblaining mates did not severely 

limil eoloiu/at ion b\ dlmoiphic s[)ccies (Sakai et al.. 

199. )a). The incidence of dimorphism is also high in 

the Hawaiian Inlands because in at least 11 lineages 

dimorphism evolvtul bom herniaj^hrodilic colonists, bloh^gy in Scliiedea, and we Ikuc us<m1 ph\ log(Mi(4ie 

accounting for about onc^ third of the currr-nl di- anal)sis and the comparatiye method to lu'ljt infer 

morphic species. These lineages, widi antocduhonous 

w ilh slnlL-> in habitat and 

chaiiires in 


e\ olulion of 

dimorphism, lendet 


to lu 



causal (actors in ihe e\()lntion ol breeding systems 
(Weller .K Sakai, 1999). 

Karli(n' |)h\logenies of Schiedea based on motpho- 

diversilicallon rates (more species per eolonlsl) llian 

t:ilher hennaphrodilic lineages or dimorphic lineages logical characters, cliloio|)lasl DiMA, and ribosomal 

(Sakai et al.. 1995a). .Vnalvsis of 

iinlicales ihal breeding syslems have evolved in ihe 

ineages also 

DNA rotriclioii-sile aiuiKsis (Wagner et al., 1995; 
Weller et ah, 1995; Soltis et ah, 1996; Sakai el ab, 
lawaiian Islands not only In ways that ])romote 19971)) lia\e been refined more recently using se- 

ways that (pience analysis of ITS and ETS gtMies and a revised 

and e\|)anded morphological data (Nepokioeff el al., 

2005. unpubbsluHl). Onl) extant s|)eci(^s were in- 
(dnded In the study so that combined anaUses could 

(til I crossing (e.g.. dioecx). Init aI.>o li 


piomote selling (WelhM' et al., 199.>: Price cK \\ agner, 

2001, W(dler v[ ah. 2005). 

While flora-hwel anal\ses of (actors associated witl 






jrecding system e\(»lLilion reveal general |)atlcrns, 
selecllve factors promoling speciation and the evolu- 


)e most evident through 

be condiick'd. Maximum |)arsimon) anal)scs were 
fXM'lormed using unweighted parsimony for the 
morphology and nuclear (IFS and f"TS regions) data, 
both sepaial(d\ and combined. iVIaximum likelihood 
searches on ihe molecular data utilized an ileralive 

lion of dimorj)hisni ma\ 

studies ol herma[)]n"oilit ic lineages that evoKt^d 
dimorphism after colonization of the Hawaiian 

Islands. We have focused on Schicdcn Chamlsso & approach lo evalnatt^ models and optimize model 

Schhxdileiitlal (Caryopli\ llaccae), a iiiomtphxlclic liii- parameters for an initial set of lives resulting from 

eage with a hermaphroditic ancestor in which 10 of parsimony analysis, and analyses \vej'c then |)ei firmed 

the ?A s[)ecies evol\ed dimorphism in the Hawaiian nndia llu' full) defined model pai'anK^ers (Ncpokroeff 

Islands. Schiedea is llu; fifth lar-esi bneaiiv in ihe el ab, 2005). PAUP='= v. 4.01)10 (Swofford, 20(H) was 

used for maximum parsimons^ and maximum likeli- 

1 largest bneag<' In ihe 
naliw flora and the mosi di\cise Hawaiian liiu^age 

with respecl lo breeding systems (W (dler et ah, 1995; hood analyses. Bayesian analvs(^s of morpli(tlon;ieal 
Sakai el ah, 1997b, Wagner el ah, 2()()5b). We have and inohMular data wove also conducted (Nepokroeff 
used a mnlti-diseij)linar\ approacln iiududing plnlo- el ah. 2005). The eonibiiied mole<-u]ar and morplio- 

Volume 93, Number 1 

Sakai et al. 

Breeding Systems in Schledea 


logical (lata sets resulted in 222 characters m- past 5 l\la, because dispersal hetween islands was 

rornuitive in pai'siniuny analysis. Using equal weiglit- pre\ iously limited by an extended period wlien only 

ing of characters, 24 most parsimf)nious trees resullctl, small, low, widely spaced islands were formed (Price 

with a length of 613. The ITS and ETS secjucnces & Clague, 2002), The current Islands widi species of 

viekled a sinH;le HkeHhood tree, and a sintrlc Ba\<'sian 

Schiedea range from the ohler islands of Nihoa and 

consensus tree was also produced, dliese trees were Kauai lo the youngest isUmd ol Hawaii (Fig. 3). bi 

highly congruent in toj)ologv with each other and widi this analysis we consider \h)loka1, Lana'i. Maui, and 

the parsimoH}- trees and are not shown here. Dio- Kaho'olawe as a single island (Maui Nui), because 

geography, habitat, and breeding s)stem divei>.ily they w^ere interconnected lor more than 75% of their 

w^rc optimized using MacCladc l.O (Matkhsnn & existenc:e (Pfice & Fdliotl-Fisk, 2()()4). Sp(M-ies in die 

Maddison. 2000) onto one of the 21 most parsinu)uious most basal clade o{ Schiedea {S. lucmbranacca Si. John 

and 5. Iiellen Sheiff) occur on the ohler island of 

although several \\eakly sufiported nodes indicate Kaua'i, and die sister relationship of these two species 

that eonchisions about the mmiber of evolutionarv is stroiigly supported. Schiedea appears to liave 

^ s 

trees showing the fewest unn-solved poKlomies, 

transitions are t(Milative. 

coloniz(M] [he older current major 


islands, and 

Sequence analysis ol ITS, ETS, /nalK, and lrfi\~V 

the ])asal clades ol Schiedea also exhibit the greatest 

has pro\idcd a better understanditig of the (wtant moiphological (h 

diversity (Wagner e 

:t ab. 1995). The 

sister group to Srhtcdea. Based on tliese analyses, llu- greater m()ri)ho]ogical diversit) in tl 
extant sister group to Schiedea is strongly sui)|)()rled 

lesc oiner c 


mav result from diversification into the greater range 

islands age and f 


and consists of a lineage c'omprised of circuniboival- of enA'ironuuMits that dtwcloi) a 

north temperate Ifonckenya prplnides (b.) Khrh. and adaptation to more diverse modes of pollination. The 

Wilhelinsia physodes (Fischer ex S(;ringe) McNeill, higher probability of exiinctioti of intermediate forms 

a species with an \laskan to northeastern Asian in 



le oKKM" cuKies may also emp 



ze ( 



(h.^tribution (\ci)okroeff et ab, 2005). Analyses of the among species 

strict consensus tree of the 24 most [tarsimonious trees 

Most intcr-isbuid colonizations appear to be from 

(Fig. 1) indicate that Schiedea is a strongly supi)ortcd oldei" to younger islands (Wagner et ab. 1995). but 
monophyletic lineage that arose from a single common a few^ back colonizations also may have occurred (e.g., 

from Kauai to Nihoa {Schiedea verLicillala F. Ihown in 
much of the ph\l(»geny is onI_\ weakly supported, Christopherson & Caum), from Maui l\ui lo O'ahu 
several areas with moderate to strong support are (several dimorphic species), and from O'ahu to Kauai 
present, including a number of well-supported species (5. spergnlina)). In most cases, movement between 

ancestor of circumboreal or Alaskan origin. Although 

pairs. In the strict consensus tree, with the exce^ition 

islands led to sullicient isolation in sjiace and time lo 

distri])utions. Scluedea gjahasa Fb Mann is a small 
subdioecious subshrid:) thai ^iirows onlv on coastal 


of gynodioeclous Schiedea apohremnos St. John, all result in formation of new species that w(M-e single- 
other dimorphic species occur in a single moderately island endemics, rather than species with multi-island 
well-supported (dade (sect. Schiedea) that also distr;])ullons. Onl) Unee species have nmlli-island 
includes three hermaphroditic sp(Mles. Within section 
Schiedea^ there is tnoderate support for a terminal 
su])clade of several dimorphic sjjccies (.S. salicaria 
lliliebrand, 5. ligusfrina Chamisso & Schlechtendal, 
S. adamands St. John, S. healiae Caum & Hosaka, and 

S. spergulina A. Cray). L nfortunalely. this section, 
which is of greatest interest in the evolution of et ab. 20051)). Two other ^peeies (5. hooheri A. (iray 
dinuHphism, Is also one of the most [joorly resolved and S, nuUallii Hooker) are both found on Oldui and 
paits of the Iree, i^M-haps because it has evolved i»iore Maui Nui ni diverse niesic f(»rest. 
rcc-cntly than other clades. Several Hawaiian lineages show inter-island colo- 

nization to }'ounger islands lollowed liy habitat 
di\ersification (\\ agner & Funk. 1995). Species |)airs 
that are well supported m phylogenetic analyses give 

cliffs (»f O'ahu, Maui Nui, and Ilaw^ail* and 

^ _ 

disperse relalively easil) betwee]i islands by rafting 
(Wagner et ab. 1995): floaling mats ol S, glohosa have 
been obser\-cd floating offshore of Molokal (Wagner 

HiocKocK \iin \\o I'A'rrKKxXS or sri-xi \ rioN 

About 10% of anglosperm colunisls in the Hawai- some indication of the importance and ddfcrences in 
ian flora have temperate affinities, including the inter-island versus intra-island s[)eciation In Schiedea, 
ancestor of the lineage comprised (A Schiedea (Fig. 2; Most species ])airs occurring on older islands are on 

the same island but ditler in halntat. are isolated 


2005. uuiuiblished). AUIuuigh 

Nepokroelf et 

islands have been h)rming over the Haw^aiian hot spot ecologically, and, in some cases, show profiounced 

for the past 85 Ma ((4ague, 1996), most colonization morphological differentiation. Species pairs on youu- 

of die current hiirh islands has occurred within the 


ger islands lend to bt; in similar habitat on ddfcrent 


Annals of the 

Missouri Botanical Garden 


S. spcrgulina 

S. kcaliac 

S. adanianlis 

S. ligListrina 

S. salicaria 
S. lydgatci 

S. halcakaleiisis 
S, mannii 
S. globosa 
S. sarmcntosa 
S, mcn/icsii 
S. hookeri 
S. pubcsccns 
S. pcn(andra 
S. nutlallii 
S. kaakic 

S. diffusa 

S. jacobii 

S. hawaiiciisis 

S. kiiii 

S. stcllarioidcs 

S. pcrlnianii 

S. kauaicnsis 

S. apokrcmnos Anestioschicdca 


S. \ iscosa 
S. lychiioidcs 
S. obovata 
S. trincrvis 
S. vcrticillata 
S. allcnuata 
S. nicmbranacca 
S. hcllcri 



Pol V no lira 


Honckcnya pcploides major 

Honckenya pcploides dilTusa 
Wilhclmsia pliysodcs 

Miiuiarlia mochringioidcs 

Minuartia rossii 

SclLM'anlhus billoru^ 



jcocarpon nimiiiuim 

Fiiiiiii.' 1 . Sliicl ctniM'tisus litH' iif 24 iMI* I ires. Two tnajor pailllimis of data were anal\ /cd coiiipri^iii^ ,s('(|iicricc dala fumi 
tu'DN A ITS and [^TS regions and moiphohtg) . Si\l\ -one ninrplioloj^Ical characlci-s were sroiccL includiti^ 13 ]V\ iscd cliaraflcrs 
|Hil)lislu*d in [)i('\ if)iis anaKses l^W rllci- el ak. 1993: W a^^rua- el ak. 1995: cliaractci-s jislcd in W agnri- rt al.. 2()0rdi). The 
sections of die uetuis ar<- shown to \\u- righl o( eaeli elad<'. Bootslrap \alue.-> jiicaler than .">()% are slH)uti akove the lines. Two 
ex 1 1 net sfxuies, Schiedea (luiplexicaulis II. Vkiiin arid S. finplexa. (I idielirand) SlitaTk are otuilled friMO die analyses (\\ agner et 
ak, 2(IOr)h). Species for- which anthorihes are no| gi\cn in die lext inekide S. lidleakalensis Maid".. S. inunnii Si. Jolm, S. 
sanueninsd l)eg(aiei- tX Shi rfk .S. kanlae \\ a\\ta . S. sfr/ldriaides Ik Mann. S'. perhna/iii W . I.. W'agnei tK WelkM'. \ lidUdiensis 
Si. John, S". ddenudfa \\ . \ .. W agner. \\ eMei- iK Sakai. Ifmn Lenvd jieploules snhsp. major { I hiokta") fiulUai (Oregon). Ilniiehen \d 
pej)li)id.cs siiljsp. dij'fusa (lloituanann) Fkilu'-n e\ X . \ , Pelrovsky (Ikillin). Miiniarlid ras.sii {\\. Hiowri e\ 11 ichard.^on) ('^raehner, 
Mi/niarlid tndehriftgioides (OCk) Malik, Sclrrdnllius InJIams tlook.k, (jeocarpoii miniinuni Maikeii/le. Figui-e adapled from 
Waiitier el ak. 2()()5h. 

Volume 93, Number 1 

Sakai et al. 

Breeding Systems in Schiedea 


S. adamantis 

S. ligustrina 

S. spergulina 

S. kcaliae 

S. salicaria 

S. lydgatei 

S. haleakalensis 

S. mannii 

S. globosa 

S. sarmentosa 
S, menziesii 

S. hookeri 

S. apokrcmnos 

S. puboscens 

S. pcntandra 
S. hauaiiensis 
S. diffusa diffusa 

S. diffusa macraci 

S. nuttallii 
S. kaalae 

S. jacobii 
S. laui 

S. slellarioides 
S. perlmanii 
S. kauiensis 
S. viscosa 
S. lychnoides 
S. obovata 

S. trincrvis 
S. verticillata 

S. attenuata 

S. nicnibranacea 

S. iicllcri 












Honckenya peploides major 
Honckenya peploides diffusa 
Wilhelmsia physodes 
Minuartia moehringioides 

Minuartia rossii 

Scleranlhus billurus 
Geocarpon minimum 


Figure 2. 

alii)reviations and ages: Nilioa fN. 

Rion-eoRra[>liic livimthesis i'ov Scliiedca u^iiig <HU' of 2^1 riiosl |)ar.sinu)nious lives reconstmch^d wilh MacCLule 
4.0 (Maddison * Maddisoii. 2000: fi-uic adapted iroiii Wagner et a!., 200.11)). Island 
7.3 Ma), Kaua'I (K, 4.7 Ma), ()-ahu (0, 3.0-2.0 Ma), Mam \ui (M, 2.0-1.2 Ma). Ha\sai-i (11. O.G-ongoing Ma). Extra-Hawaiian 
(EH). Fmspeeies wilh miilli-island distrihulinns, coding indirates tlie island where it is likely ihal ihe species (nol\ed. 
Fqnivoeal n^gions are indieat<-d in gi'ay. 


Annals of the 

Missouri Botanical Garden 

/^%^ )Kaua\{4J) 



Ni'ihau (5.2) 

\0'ahu (2.6-3) 

Moloka'i (1.8-2) 

Maui (1.2- 1.5) 

Lana'i (1.5 

Maui Nui 


Hawai'i (0.6 - ongoin 

Im-ihv 3. M;i|) ..f llir Ilawaiuiii I^ with ishmd a-c iii niillioiis of years. Mima (7.:^ Ma) ort-Lir.s to llic of iIk 

islands shown. 

islands and >hou k-^:. moipludogical diffcivntiation. Wcllrr t.ii Maui Nui and llie island of IlauaiS). One 
On llie older island of Kana'i, .S". mewhramiccu, ])air occnis in rnesic Iialnlal (.S. petilundra W. L. 
a perennial hcrl), occurs in the niesic foresl of se\ei-al 
valleys, while closely related ,S. hrllcri is a vine found 

V;^iiiner e^ E. Harris and .S. puhcsrrns WiWrhviuul on 
O'ahu and Maui Nui, respeclively), and one pair 

at higher elevations in wet montane for(^sts. In ihe foin" occurs in (h'v hahllals (S. sprrgnllna an.) S, hcuJinr on 

species of the fonner -enus /l/.s7///V/e//J/v;// H. Mann. Kaua-i and O'ahu, respectively). Although Loth S. 

inter-ishmd (h'spersal precedes! (hflerentialion in liguslnna and .S. adanuinlis 
habitat. On Kaua'i, S. vlscosa II. Mc 

occur on 


HI HI (Irv 

iiui aiii 

I S. 

lycIiiH)i(l('s I lilhd)rand an 

I 1 

ci.v separated t)y elevation 


ir g(M)graplncal sejiaralion ny 


and hahilat, ah hough there is some geographic 

o\ erlaj). Srhiedca riscosd 

liahilats. there is clcc 

moLintain langes. Schiedcii ligustrina ocu'urs through- 
out the W'ai'anae M(nmhnfis (fornied 3.2-2. S Ma) in 
occtn-s at slighll) lower western O'ahLi In dvy forest lo ihverse mesic furesU 

elevations in (]iverse niesie forest in iiinilcd areas, ()n(Mi ()n (liffs. .SV/mcJc^/ aJr///?^/////,v occurs in a sind 
wlnie S. lychnoides occurs ihrouu-hout hial 


ugner (Mcvation 

popuhuion on sl(M^p dry sh)pes of open shiiihland on 
wet forests on Kaua'i. On O'ahu, S. ohorala (Shcrffj Diamond Head crater in southeastern O^ihu (h.iined 
W. 1. Wagner & WVIler occurs in mesic forest at about 0.3 Ma: Juvik <.K juvik. 199H). More definilive 
louer elevalitjns throughout die Wai^anae Mountains, hiogeograplneal |)atLerns of other Scliicdca sp<'cies 
while .S. liincn-is (II. Maim) Pax cK' K. Hoffmann is auail hellei" resolution of dieir plivloorend ic relation- 



I onl) ui hi 

n nigher ele\alIon wel forest in 





al ^ 


northern W^ii'anae Mounlains. in the five species 
])airs f)n Nounger ishmds, hoth species occur in slmihir 
liabitals, bul gtn^graphical is<jlation has occurred 
dirough disp<a-sal to <liflerenl islands or mountain //a/(y//7c//.s/.s I lilhdnand mav have otdv n^cendv shifted 

'\erat s|)ecies may be undergoing directional 
selection f(tr greater fitness in dry en\ IronnuMils 
coloni/(Ml rehiti\('ly recently. For examph'. Sclncdea 

n dv) , high light 

ranges on tlie same islantl (or h.rmer island in the case from mesic to dr\ habitat. [| oetau's i 

of Maui Nui). Twt) of these pairs occur in wet lial)itats en\ ironnients, bul exhibits morphological lialts (large 

{S. jarohii W. L. Wagner, Weder & Medeiros and 5. 

hiul W. L. Wagner & Wellcr on Maui Nui (Maui and 


Moloka'i, respectively); ihe two subsp(H-i(\s of ,S. 




\. Crav, S. 

sid.)^p. diffusa and S. 

dijjiisd subsp. nuurari (Slicrlf ) W. 

L. W agner tK' 

leaves, open pendent innorescenees. vining habit) and 
t)h\siologica] traits (maximum levels of photos\ nthe- 
sis, water use eflici<Micy) more eharacterislic of mesic 
site species (Mishio et al.. unpubli.shedj. On younger 
islands, ecological (h"\('rg(aice of species may also be 

Volume 93, Number 1 

Sakai et al. 

Breeding Systems in Schiedea 


liiniU-d by ihe later(level()[)rnent of gei)l()gical If-alures ln(]rp(^M(l('iil evolution of (liiiiorphihm is associated 

creating drier Iial.itats. Wet habitats are present on witli a slnfl to dry hahilal. All ten (limori)liie species 

voun^er islands as soon as they become Ingli ennngh occur in dry and windv habilat and most heniiaphro- 

to intercept moisture-ladeti tradewinds, l)ul the drier ditie species occur in mesic lo wet habilal. Four 

leeward slopes and (difls preferred by many Schiedea hermaphroditic species also occur m dry habilats, 

s[)ecies develop (tnly afti-r (erosion and/or sLil)sidence a 

ldi(nigli Schiedea lydgalei may be hermaphroditic b^ 


as the islands age (Walker, 1990a, 1)). 

1 Mirrvr shifts \\d cnA.\(,Ks in nuKKDixr; systk.m 

on in breeding 

reversal. This pattern, where all dimorphic species as 
well as a h-vv hermaphroditic species occur in dry 
habilals (e.g., S. menzicsii Hooker, S. handiiensis, and 
5. verficilldia), suggests diat the shift Lo dry whidy 
habilats jjreccdes the shift in breeding systeiTi lo 

The sjjectacular ada|)tive radiati 

systems in Schiedea a[>parendy evolved within the (lim<»rplHsm, but thai the evokillon of dimorphism is 

past 5-7 million years. The association of changes in not ine\itable after a shift to dry habitats. Oticc ihe 

breedinti system vvitli habilat shifts has made it shift in habital has occurred, selection may simulla- 

difficuh to discern cause and effect, i.e., to delermine n(M)iis!y favor the evolution of dinior|»hism as 

if changes in habilat ha\e driven shifts in breeding a mechanism lo promote outcrossing as long as jiolh-n 

hether shifts in breeding s\sletn have is not limiting for females (Weedier el ah, 199(5). Ihe 

evolution of adaptations promoting wind podination 

svstem. or \s 

allow e( 

1 movement inlt) new habitats. Based on 

character optimization, ihe aneesUtr giving rise to becomes crilical with the loss of biotic j)()llinalion 

Schiedea appears lo have l)een hermaphroihllc, and limiting pollen dispersal in these habitats (Rankin el 

the ancestral habital oi Schiedea was most bkely ah. 2002). Alternatively, w Ind-faciihated selfing may 

mesic forest. Although Houckenya peplnides is di- evolve luu-ause of low j)ollen production, as ni .S. 

oecious, Wilhelmsia Rchb. and other close outgroups /kncamv/.s/.s, a herma[)hrodilic- (Iry-site species derivecl 

are hermaphroditic, and il appears that dioec) \Nas from a Hneage of mesic-wel forest sjiecies with h)W- 

(h-ri\(Hl independently in Houckenya Ehrh. and also pollen production, 
wilhin Schiedea (Fig. 1; Nepokroeff et ah. 2005). 

Dimorphic breeding systems appear to have been Ski.RCTIVK Factoids l^ rUK EvoMTioN oK Dj,\U)i{lMllSM 

derived independently twice in Schiedea— \\\ 5. ^^|, Ski.kinc; 



em no 

s and once in section Schiah^a. \\ itliin 

section Schiedea. it api)ears that 5. lydi^dlei llillc- 


>reecnni!: depression, M'lfing rates, and resource 


lirand is hermaphroditic by reversal, possibi) ihrongh allocation are all factors ihal can learl to clianges in 

loss of females during 

colonization of lV]oh)kai. 

breeding s\ stems by fa\()ring either selfing or, 

Facuhative autogaui) has evolved three times — once alleruativeiy, the separation of ihe sexes and the 

evolution of dimorphism \]\ these species (reviewed in 

in the former genus Alsinidendron, in the si)ecies pairs 

S. jacohii-S. laid, and in S, hawaiiensis-S. dijjusa. Sakai <S. Westneat, 2001). In cases with nuclear 

inheritance of male sterility, as in Schiedea (Weller & 

Each of these groups with facultative 

autoiiamv has 

also evolved (»bligalc autogann (S, diffusa subsp. Sakai. 1991), tlieoretical models suggest that strong 

macraei, 5. laid, and .S, trinenis). I^volulmn of selection for dioecy ma) occur as a mtH-hanism to 

auloi^amous breeding systems is also linked to promote outcrossing (Lloyd, 1975; Charlesworlh & 

changes in habitat. Diversification into wet habitats Charlesworth. 1978; reviewed in Ceber et ah, 1999; 

has occurred indei)endenlly five times, and in several Welhn- & Sakai, 2005). If inbreeding depression (5) is 


f ihese cases, a shift to facultative or (obligate 


Ifed progeny of hermai)hrodites will have 


autogamy has occurred. Idie repeated independent lower filness than progeny derived from outcrossing. 
e\olutlon of auti)uam\ with wet habitats ma\- result Unisexual indi\ ichials, usuady females, wi 



that are less 

from historicallv small j>opulation sizes in these favored because they prodnc(^ unit rossed progcMiy 

with selection for closed pendent flowers with relalively higher fitness than ihe selfed progeny 

likely lo be adversel} afh-cted by of hermaphrodites. Under the simplest conditions, 

extremely wet conditions (Weller el ah, 199o; Wagner females wid be favored if /. + ,sS > 0.5, where k is ihe 

et ah. 20051j). Some exceptions occur to these seed production of females r(^lati\e to liermaphrodiles 

palt(M-ns: S. helleri nccyu> in wet monlane forest, but {k = O if hnnales and herma[)hrodiles produce e(iual 

shows no inchcation of autogamy, and S. haicaiiensis numbers of seeds) and .v 1> the selfnig rale. Because 

inbreeding (with selfing as ihc nio^t extreme (orm of 

occurs in dn^ fori^^t. but is autoganuHis rather than dio(H'ious species produce only unisexual iiidividuals, 

sexually dimorphic. 

Evolution of dimorphic breeding systems is also inbreeding) is much less lik(dy in dioecious species 

linked to changes in habital (Fig. 4). In bolh cases, the than in lua-maphrodilie spc^cies. Se])arate sexes may 


Annals of the 

Missouri Botanical Garden 

S, adamantis 
S. ligustrina 
S. spergulina 
S. kealiae 

S. salicaria 
S. lydgalei 

S- haleakalensis 
S. mannii 

S. globosa 

S. sarmcntosa 

S. mcn/icsii 

S. hookeri 
S. apokrcmnos 
S. pubcscens 
S. pentandra 
S. hawaiiensis 
S. diffusa diffusa 

S. nuttailii 

S. kaalae 

S. jacobii 
S. laui 

S. stellarioidcs 

S. pciimanii 

S. kauicnsis 

S. viscosa 

S. Ivchnoides 

S. obo\'ala 

S. trincrvis 

S. verticil lata 

S. allcnuata 

S. mcmbranacca 

S. heller! 












S. dilTusa macraei oa 
















I W 

I M 

[ W 

I D 


I W 

Honckenya peploidcs major 

Ilonckenya pcploides diffusa 

Wilholmsia physodcs 

Minuartia moeliriimioides 

Minuartia rossii 

Scleranthus biHorus 
Geocarpoii niininuiin 

M^iiir ]. 

Btvcdiiin, syslciii ('voliilioii li\|.o|lH-sis for Schicdea iisiiin; onv of 24 nif>sl [KirsinioMiniis Irres ivconstruclrd wilh 
MacClad.- l.n (Ma<l(li>c>n .^ Mad.lis.m. 2000; inodifit'd Ciom \\'ai;i]( r r\ al.. 200:)I.). I lal.iiats ofsprrirs aiv -Iw.un in die [»ar lo 
rh." ri-lil. K((iiiv(Kal ivoinns fnr I, n-rding syst<'nis aiv indicated in -tax . llal.ilal>: 1) = dv\ .sloprs a.ul cliirs: M = Mesic fnrvsl 
and; W' - WoL (on-sl. Rreedni- s> - = gyn.,di,.rci()us; d - dioccion.-.; sd = snlHlloc-Ious; 1. = 
hrnna|)lirodi[if; la = facullal ivcdy autogamous; oa = i^hliiialtdy aiiloi^anious. 

Volume 93, Number 1 

Sakai et al. 

Breeding Systems in Schiedea 


of iiihreediiig depression expressed in the field over 
more llian one flowering season in presumaljl) harsher 

also be favored in die absence of hii^h inbreeding 
depression and high selfing rates if females compen- 
sate for the lack of nude function (pollen production) field conditions, 
by producing more than twice as many seeds as 
herma|)hrodiles (/.• = 1; Charlesworlh & Charh^s^vortln 
1978- Llovd, 197S). A comf)ination of somewhat br(;eding system. It is a pcrcimial herb endemic to 
greater seed production by females and higher levels Kauai diat grows in mesic environments typical of 
of selling and inbreeding de|)ression may also promote hermaphroditic species. Schiedea mcmJmtnarcd has 

a hiuli level of outcrossing (low selfing rate) that 

Schicdcd wernhranacca is a member of the basal 
clad(^ of the lineage and has a herniaphroihlic 

separate sexes. 

Kesource allocation [o primaiy sex traits such as prevents expression of the high inbreeding dei)rossion 

biomass of pollen and seeds will obviously change 
with the introduction of unisexual indi\ iduals in 

detected lollowinii controlled crosses in the green- 


house ((udley et ah, 1999). Measures of geucti( 

a population of hermaphrodili^s (i.e.. die evolution of diversity (number of alleles per h)cus, percent of h>ci 

from hermapln-oditistnj. dlie polymorphic, and percent luatirozygosity) also are 

gynodioecv and 



challenf^inii nroblem has been to discover if consistent with other oulcrossing s[)ecies (Weller et 
these changes in resource allocation i>atl(M-ns are the al. 1996). Schiedea weinhninacea is apparcntl) 

(U'lx nig 

force in the evolution of separate sexes, with biotically pollinated, witli a relatively low i)ollen : 
sul)sequent changes in inbreeding depression and ovule ratio and an open inflorescence (Table 1). 
selfing rates, or allernati\(dy, if changes in selfing Becaus(^ of the low selfing rale, expressiuii ol 

rates and inbree(Hng depression occur first. Tlie order nibrecding depression is low, and the hermaphroditic 
of these changes is difficult to deduce in dioecious breeding system in this species is a|)pareiiHy stable, 
species, where changes bodi in resource allocation \\\ amh-d^i U) Schiedea jucmiivanacea, S. riscos<} \vc\^ 

and ill levels of inbreeding and inbreeding depression a stable liermaphroditjc breeding system because it 
already have occurred. Cynodioecious species that are has a high selfing rate, but much of the inbreeding 

de])rc>sion characteristic of outcrossing speci(^s lias 
be(Mi eliminated from tliesc^ ])opulations (^\ eller el ah, 



under conl inning selet:tion for ctianges in uie 
fre(|ueucy of females may ofha- more insights than 
dio(M'ious species inlo the factors imporUml in die 2005). Tyi)ical of populations that are historically 

selfing. the pollen : ovulc' ratio is extremely low, and 

also has very low measur 


es of g<Mi(4ic 

evolution of both gyno<lio(^cy and dioecy. 

Cotiiparisons of six species oi Schiedea species give 5. nscosa 
some clues about the rehuive order ami importance of di\ersity (Table 1). Schiedea nscosa (formerly m the 

changes in inbreeding dej)ressioiu selfing rates, and 
seed production with ihe evolution of breeding 

systems m 

I99.S. 1997; Sakai el ah, 1997a; Culley el ah. 1999; 

genus Ahinidendron) is a rare hermaphrochiic vine 

thai occurs in mesic habitats ol' Kaua'i. The flowf^rs of 

this hnea-e (1able 1; Norman et ah, S. viscosa are pendent and rtauaiu relatively closed, 

liaits thai may be adaptive in rainy conditions and 

lutioii of selling. 

Rankin et ah, 2002; Weller & Sakai, 2005; Weller et ihat may have promoted the evo 
ah, 2005). Measurements of seed prcKhietion were 5r//Wcr/ /v.sYmY/ also pnulut-es nectar (0.64 )il/fl()W(M7 
taken from ficld-eolleeted inflorescences. Selfing 24 h in die greenhouse), suggesting an earlier history 
rates were measured u>ing starch gel elcctrophfiresis (»f biotie pollination (Weller et ah, 1998). 

Two gynodioecious specie^s illustrate the changes 
thai ma\ occur with an increase in the fr(^(]uency of 

the trreenhoube from field- 

on progeny grown ni I lie green noube 

collect(Hl seeds. Recause most field sites occur on 

remote steep cliffs, levels of inbreeding depres^^ion fenudes iti i)opulations. Sr///We^/ .sYi/icami, a gyn()(li(>e- 
were measured in the greenhouse on progeny resulling cious speci(^s with a low frequc^icy of females (K^%), 
from controlled crosses involving self and outcross 
pollinations. Trails used to calculate inbreeding 

is f 


in dry windy liabilals of the West Maui 

Mountains. Schiedea adamanlis is also gynodioecious 
de[)ression included the number of seeds pta-capsnle wilh a higher frequency of females (39%). and is 

found on llu^ more recent dry slopes of Diamond Head 
Cjater on O'ahu. In thcs(^ two species, greater 
dilfer<Mitialion ])elw(;(in females aJid hermaplnodiles 
priinary and secondary sex traits occurs in 5. 
a proportion of \alu(^s for outcrossed progeny was adaniafilis (Colonka et ah, 2005). In 5. salicana, 
calculated for each trait for each family and used in femah-s and hermaphrodiles show oidy slight differ- 
entiation in lh)ral and inllorcscence traits and nearly 
alculated as J-relative fitness. Our in- identical seed production (Weller & Sakai, 2005). In 

5. adamanlis, females produce 2.3 times more seeds 
than hermaphrodites in the field. This occurs liecause 

following die controlled pollinations, pcrceul gcami- 
nation, percent survival until flowering, and idther the 
number of flowers p(a- inflorescence or infloi-escence 
biomass. The relative fitness of selhnl prog(aiy as 


a Mudliplicative fitness function. Inbreeding depres- 

sion was c 

breeding depression sludies of these ])en^uiiial plants 

in the greenhouse probably underestimate the levels 

Table 1. Ilahitat. breeding system, .sdfiiig rale, inbreeding depression, an. I differenees In resoLirc(> alKnalion fur six speeies of Sc/uaiea. For see Norman et al 1 W7- W rller <-t al 
109G; CuIIey rl al.. 1999: Hankm et ab. 2U(12: W rller et ab. 2.H15. Resntnre alloralion difference, bet^se^-n feniale> and b<-rmaphn>dites ..annot be eaU-ulated m bermaphrodife species. Xumbr.- 
of llouci- prr -nnorescence and ninorescenee ennden>ation ucre not mra>nred in 5. rlscosa. binorescence condeu^allon i. the nu.nber of nowers/innorescence/mnore.eenee b-nwb in cm. Small 

populations are < M) nunviduals: large popidalions are > ]()() individual... E.limates of genetic di><-rsity (mean number of alleles per locus, percentage nf I 
be(erozygosily) were !>ased on 2 1 to 39 planis per poptduliou (^\\dler e[ ab, ]996). 



Hreedinii .-^v >ten 


()\nle (N) 
Pollen (N) 

\ / 

P:() ratio 
I'ollen si/e (p) 

^ fi/mno 

billorcsccnce leiigdi 


INcclar (^b/2 I li) 

ScKniii rale 

nhi'eedmg drpression 


Pnjnilation si/e 
Mean \ alleles/1* irus 
% o{ loci pol\ tnor])bic 
Mean betero/ygoslty 

^. nicnihrdnficcfi mesic 
forest herb 








■? ■? 









slable; outcrossing 

S. ii'srosa mesic 

foi-fst \ ine 





3 J 22 





(presumed 1.0) 







stable: faeuhaii\e 

S, sahcana dr\ 
shrubland ..hriib 

g\ nodioeeious 

(13% F) 








30, 1 







no dilierence 



Fanrl H 


/ i .8 

unstable: selection [o 

S. (ulamdutis dr\ 
shrubland shrub 


39% F) 


22. J 7 



51 .5 









pi"oduce 2.3X 
seeds than 1 1 

1 a rge 




e; se 



foi- femalt^s 

oci poi>"morplnc, and mean 


^S. menziesii {\v\ 


shrultiand siniib 


not ada|)ted to win 












mr^lable; selection 
fnr females 

S. I\ (lii-alei dry 
shrubland shrub 


biotic (moth) 



















stable: outcrossiuii 
hernia] ibroditos 











Volume 93, Number 1 

Sakai et al. 

Breeding Systems in Schiedea 


suggests lliat the evolulion of autogamy is unlikely, 
even with high selling rales. 


Scliicdea lydgalci is another hermaphro(h'{ic species 

habit als on Moloka'i. and based on 


] I 

n (H'v 


females and herniaphrodiles produce similar numl)ers 

of infloresc^Mices and riowers per in(h)rescence in the 

field, but females produce (ar more capsules per 

iuHorescenee than hermaphrodites (Sakai et al., 

1997a). Schiedea adamanfis also shrnvs much greater 

ada])lali(in toward wind pollination, with a higher 

polltMi : ovule ralio, smaller pollen grains, and more system. Unlike S, m.enziesii^ S. lydgalel lias a low 

condensed inlloi-escence than 5. salicarui. Schiedea 

sdlicarid, ah hough winrl pollinated, has pollen : 

j)h) logenelic e\id{Mice, appears to l)e hermaphroditic 
by reveisal bom a sexually dimorphic breedin 


selling rale, which limits ex|)rcssion of the high hnels 
of inbi'ccdlng dt^pression found in this species. As 

o\ule ratios, polh'n grain size, and inflorescence a consequence, the breeding system is stable despite 
architcciure more similar lo biotically pollinated 

species (W eller et ab, 1998; Golonka et ab, 2005). 

the high inbreeding depjession levels. Schiedea 
lydgalci is apparently moth-pollinated (Norman et 
Schiedea salicarui and S. adamautis also differ in ab, 1997), and the occurrence of biotic pollinatioji 

Is of selfing and inbreeding depression. Schiedea 

levers oi se 

salicaria- ha^ 

av 1 

4 4 

I i 

mav ne critical in the maintenance ot high ontcrossnig 


s a m 

ixed mating system, with a high rates and hermaphroditism. 

selfing rate (0.7; W c^lh^- & Sakai, 2005). but with 

Tlu^ jiatterns of inbreeding depression, selfing rates. 

exlremelv high inbreeding depression (0.8; Sakai et and alloc-alion shifts in these six hermaphroditic- and 

al., 19<-!9). Th(^ low frecpiency of females in 5. salicaria dimorphic species suggest that [he evolution of 

is con.^istcnl with ihese estimates, although if selbng dimorphism is associat<Ml with a shift to dry, windy 

and inbreeding depressiitn liave been underestimated habitats atid the evolution of wind pollination in 

in these greenhouse studies, selection for increased Schiedea. The colonization of windy, diy hal.)itats 

re])rt:senlation of females may l^e strong, bi contrail, appears to occur before changes in sex allocation. For 

S. adamantis has both high selfing rates and high most herniaj)lir()dllic species, die shilt to dry, windy 

habitats apparently is associated with a loss of insect 

inlneeding depression (Sakai et ab, f997a). bi 

combination with the greater seed production of jxdbiialors, r(^sulting in an increase in the selling rate. 

females, th(;se rates of selfing and inbreeding de- 

The increas(Ml selfing rate may result in greater 

pressioii suggest strong s<dcetion for females in S. expression of the high inl)re(Hling depression rates 

ac/aA7K/n//,v. Tlie [)re(licted fre(juency of females (based found in these historically outcrossing i)opulations. 

on Llovd, 1975) is 42%, remarkably close to ihe \i\\i\cv tlies(^ conditions, females could be favored 

observed frequ(Mic) of :V)% (Sakai et ab, 1997a). The becausi; ilu^y are obligaiely outcrossing, but only il 

low esliinati^s of genetic diversity in S. adamanfis pcjlliiiation is not limiting populations (^ eller et ab, 

suggest a severe population bottleneck in the past 1998). bi these laivironments, the evolution of wind 

(Weller el ab, 1996). More recently, the size of this pollinalion may be f(tllowed l)y the rapid appearance 

population has fluelualed widely over the past of f(unab;s in po|>ulations. Once females are in- 

20 years, from a high of about 400 flowering plants troduced into (he p(»j)ulation. there is strong selection 

to a current low of 2 |)lanls because of extcndtnl (or different allocation patterns favoring hermaphro- 

ditt's with urcaler male function, bi these dry hal)itats. 

selection mav act on traits associated with wind 

jolliuation and/oj- simultaiUMJUsly on traits associated 


allocation to increasiuijlv male or 

drought and eoiiipclition from alien species. 

Schiedea njenziesii, one of the few hermaphroditic 
Schiedea species growing in diy habitats, may be 
under selection for e\'olution of sexual dimorphisiTi. with resourc^e 
Unlike other *h\ site species, 5. menziesii does not female function. 
appear lo be well adajjled h)r wind pollination (e.g., 

low pollen :o\ule ratio) and shows no evidence of P()TKNTIA1. FOUfti]: E\i)l.L HON 01- DiMoinMiiSM 

wmid polbuallon in a wind luimcl (\\ eller et ab, 1998). 

This speci(^s has both high inbreeding depression and Theoretical models suggest that the evolution of 

high selfing rates, conditions that (avor females in dioccy may be favored becauseMnbreeding depression 

populations (Table 1; Rankin et ab, 2002). Females 
occasionally occur in neld-coUected seeds grown in 
the greenhouse^ but have not been detected in the 
field. Greenhouse crosses suggest that these females 

levels and selbng rates are both high or because shifts 
in allocation of resources to a single sexual (unction 
result In accelerating fitness returns for indi\'iduals 
(Charleswortli & (4iarlesw(nth, 1978; Charnov, 1982; 

are a restdt of a mutation for male-sterility (Weller & Lloyd, 1981). These accelerating fitness gain curves 
Sakai, unjiubhshed). Without biolic pollinators, 

may resull from a variety of ecological factors, 
inclu(hnir specific dispersal agents and shifts in 

females may not be able to establish and increase in 

tile j)opnlation withoul adaptations to wind pollina- pollinators (revIew(Hl in Bawa, 1980; Lloyd, 1984; 

tion. '\\\c lack of adaptations for intrafloral selfing Thomson t'l RrumM. 1990; Sakai & Weller. 1999). In 


Annals of the 

Missouri Botanical Garden 

Schirdcd, sliifls lo wind [xillinalioii, as well as lii-^li 



iiniit'ccuii^ depression and ini^h scaling rales, appeal 


lierilahilitv ef l)ioinass alloeaLed le male and female 
fnnelioii in {^Niindioeeioiis species. Sij^nilieanl luM'ila- 
to he strong selective pt('ssnres ra\()ring the evohilion hllily of hioniass would indicale ihc potential lor 

e^'oluti(^nary ehani:;e. assnniinp; I hat genetic correla- 
these selection pres^[n■es with furUier evolution of tions do uol otlier\\ise constrain the response. Vi'e 

of gynodioecy and dioeey. The ahility lo respond to 


'e(lni<; systenrs will (lepeiid upon the genelu 






a (|uanlilall\e genetics approach to 

[)olential h>r changes in allocation lo male and female examine the genelic potential to e\ol\c new hrcediug 

hinction. systems and trails related lo allocation to male and 

All of these tnodels assume the existence of female function in iiMiodioecious S. salicdria. a sue- 

herilahle gent^ie varialiou in |>allenis of allocalion cl(^s willi 1.'?% hMuales, and in .S. r/J.'////a/;/,/'v. a species 

with 39% IcMiales. 

^c used lietcro/.)gon> luMinaphrodites and females 
as parents to generate faimdies thai woidd piodnce 

eolls \\\ 

lo male and fejiiah' nnieliou. Cenetic had 
allocalion helween ihe two sexual fmictitMis arc also 
assumed (Stanton v^ CaMowa\. 1990; CharlcNWorlh c^ 




1991; tv\iew(Ml in r,(d)er et ah. 1999). holli iKM-maiduodUcs and female progenw in Schicdea 

1 sahcariiK diirl\-(i\e faimlies (each c(tnsisting of one 
helero/ygous h<M-maj)hroditc and one rchUiHJ lemah^) 

^^^l:ati\e iienetic corndalious ]}ctweeu iiune an( 



female I raits, such as slamcn hititnass and 

hiomass ni heitna[)hrodil(^s, may enhance the evohi- were used in pollinations to [)i-oduce ihe plants for 

lion of dioeey, whih- posilivt; gtau'tic cori-(dati(nis 

lietweeu these trails would impede evolution of dioec) 


a singh^ general ion ex])erimcnt lo (\stimale the 
lerilahi lilies and genetic covariances for ihe focal 


ower si/e. 

\\^' know htllc ahoul palterir-^ of genetic \'arialion 
ami cn\arialion in charaelers relalcd to sex allocalion 

and urstead impl\ selecliou U)v larger or smaNcr traits. We (Mtiployed a parlial diallel design sinular to 

that of Meagher (1992), hut Avitli larg(a' ^^ample >i/es 
h)r greater stati>tical power. Rach hermaplu'odile was 
used as a [Kdlen donor and crossed with tluxH^ lemales 
(or natural jiopidalions. Old) a h-w nn-ent studies ha\c randond) chosen from different famili(^s. and each 
e\plore<l ihc (juanlilal!\ e genetics of sex allocation female was crossed with three diriercnt unrtdated 
trails ui herma]}hroditie [»huit spiM-ies (van [No<>i-d\\ i jk hermaphr()(litt\s. In mosl cases, five females and five 
<!( de Jong, 1906: Slanloti c^ (wdh)way, 1990; I Ionic, hermaphrodiles from (Nich sihship were measiucd for 

1991; OWeil c^ Sclunill. 1993; Agren & Sehemske. 

more than 30 trails. Additive genetic \arianc(\s were 

199S; Delesalle lK Ma/.er. 1993; Ma/er tK Dclesalle. estimated separatel\ for females and h(Miuaphrodite< 
1996; Camphelh 1997; Mazer et ah. 1999). These hv 


exanuiutig die component of \aruition 



sludies used controlled cn)ss(^s to create familie> lo palernal lialf-.-^ih families using reslrieled maxiniLuii 

ikelihood methods (sec^ Kearsey, 1903; Shaw, 1987; 
eaglier, 1992). Nai'row sense heritahililies 


cslimate genelic varialiou and covarialion (»f uKupho- 
logical characters, hul llu^y gen<a-ally were uol |)laeed 

in a phylogenclic conlexl. Other slmhcs have calculated for each trail in eacdi s(^x as ihc adih'live 

exarmned ihe quani ilali\e getu^ics of sex allocation g<aie|ic variance (four limes the palernal \ariance 

trails in gyuochocciou.s (Ashman, 1999. 2003; D(d|>h com|)onenl for this design) divided hy the lolal 

el ah. 2004, 2003), andromouoecious (Fdlc. 1998). variance (pat(^rnal variance + niatia'ual \ariauc(^ + 

and dioecious sjiecies (Meagher, 1992, 1991). Facu error: Falconer iX Mackav. 1996). Genetic co\ ariauees 
fewer sludies lia\e examined ihc (pianti tali \ (^ genetics and coir(dat ions were (estimated separat(d\ lor females 
(t( physiohtgical traits in g\riodio(Maous sp(M*ies (Fon 
et ah, 1996; Caruso et ah, 2003). 

arul hermaphrodites, using hest linear unhiased 

predictors (15FL l*s) of sire 1 

re [)|-eeduig values ohtained 

Closely |-elated sp(H:ies of Scliicdea wilh diff<M-enl from our Vnn- Mixed analysis (SAS, 2001; Conner et 
j)r(tpoiiions ol hanalcs and with \ariation in male ah, 2()()3>). Pearson corridalion coefficients helwt^eii 
hnulion in hcj-maph rod lies should he esp<'eiallv 

HFFFs were' cahadaU^l fore 

acli sex. T 

ic icmale an* 



f ll 

oitnalive ni shuhes ot ihe genetic cnauges uu- 
derl) ing these sex allocation dilfercnces. In Schicdca, 
male sterility is coutrolle( 

(Weller & Sakai, 1991), hul (luanlitative variation in 
other traits related lo sex allocation in females and 

h\ a single nucdear <xrn(' 

hiainaphrodilie data sets were also comhined and 
Pearson correlation coefficients were; cahadaled 
hetween homologous traits of the two s(^x(^s. 

Ilentiibdilies, and genelic correlations of frinalcs 
and henn(ij>hn>dii('s of Schiedea salicaria. Mosl 
hermaphrodites is liki'ly lo he eontndl(Ml hy a munher floral trails show significant heritahiMlies in hauah's 
of genes. Some gynodioeeious species ma} ha\'e 
hrtuuliug systems that are in hansltion. with al local inn 
])atlerns that ar(^ under direclional selecti*tn. (/i\('U 

and hermaphrodites. In general, the floral hiomass of 
stamens (measured only in hcrma])hrt)ditcs) and 
carpels in hoth s(\xes shows high lua itahililv. Fruit 

this rang(^ ol hitHaling systems and all(K-ation patlcirrs hmmass is uol herilahle in terminal llowcrs. hut is 
ni sLudi closely I'fdatcd spfH'ies. we expecl sigtuficanl herilahle iti the more muutaous latei'al flowers in holh 

Volume 93, Number 1 

Sakai at al. 

Breeding Systems in Schledea 


sexes (Sakai el al., unpublished). At the iiil'loi-cricence the genetie potential fur diflerenl breeding systems to 
level, botli females and hermaphrodites exhibil high evolve in Schicdea and the selective factors that have 
herilabibty in [lie number of flowers and fruits per proinoled specialion and shifts in l)rceding systems. 

dimor[)hism evolved independently 

inflorescence (Welh;r et aL, in press). These results Autogamy and 

suggest that significant genetic variation is ptx^senl in several times in Schicdea^ and diversification has been 

lis s|)ecies and tlial a response to selection coidd associated with changes in breeding system, pollina- 

resuh in further differentiation of (eniah^s and ijon system^ and habitat. In general, dimorphic 

liermaphnKhles, deptuiding uj^oii genetic corrchitions species have evolved in dry, windy habitats and are 

of traits. wind pollinated, wliih; auloganious species occur in 

Cenclic correlations within hermaphrodiles arc wettt.'r habitats. Dimorphic bree(hng systems may have 

bed a? 


evoh en as a mecnanism to promote outcrossnig 

indikely to [iromot*^ or hinder tlie evolution of (hoecy 

in this s()ecies. ^\'ithiii hermaphro(ht(\s, ((Miude bio- l)ccause of the exjiression of high levels of inbreeding 

mass f()\ary. fruit, or seed) and male (stamen) blomas^ (h^pression resulting bom high selfing rates that occur 

are iruh-jHMKh'nl of each other. Female biomass in ^ith the loss of pollinators related to a shift to drier 

females and male biomass in hermaphiodites also habitats. Quantitative gent^tics studies suggest that 

shou(Ml no genetic correlation, suggesting thai spe- i^^^st morphological traits associated with wind 

pollination and resource adocation are heritable and 

ciali/ation toward greater female function in femah^s 
and greater male [unctit>n in ]ierma[)hro(btes would 
not be constrained. Other genetic coriohilions may 
impe<l(^ selection lor sexual dimorphism, uidi po^iliv(^ 
genetic correlations between similar trails in femah^s 
and hermaphrothles. For example, the female biomass 
of females and of hermaphrodites is sigiiilicaiilly 
genelicall)' correlated, making speciali/atif)n more 
(hflicuU (Sakai et ah, unpublished). 

Schivdcd sdHcarid has likely undergone a recent 
transition bom biotic to abiotic wind |)ollination. and 

could respoTid to s(dection. Strcuig selection for 
outcrossiiig in di'y ha])itais and for selling in wet 
habitats suggests that a bn-|lier response to selection 
in 1)reeding systems and other tiaits is possible. 

[jleralure Cited 

Agrcn. J. & D. Vi\ Sclicniskc. 1995. Sex aliocatit^n In [lie 

herb Begonia sriniovdtn. Fvohitinn 49: 



* 1 ♦ * 



sigTiificanl narrow-sense l"ientai>ililies were detectec 
U)v inllorescence condensation and other traits ridattnl 
to wind pollination in Scluedea species (W'eller et ah, 
ill press). Herila])ilities w^ere generally higluM' in 
hermaphrodites than in females. The presence of 
signibcant narrow-sense heritabilities for traits asso- 
ciated with wiin1 ixillination suggests that selection for 
more effective wind pollination in llu; windy, Baldwin, B. C. 20U."i. A pliyU)gt;nelit' perspective on ihe 

pollinator-limited environments where S. sdlirana 

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f morohol 

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internal barri<-rs to gene flow across lineages tlua-ein. I{esult> of recent investigations have shown that highly dynamic 
e\olutionar\ change in ^hldiina(^ hotli in [tlienolypic characters and in modes and jiatterns ftf diversification, i-xtcnds to even 
in(a--scale evolutionar\ levcds ihan indicated hv Clausen et al/s (dciran 

1 hy Clausen; 

^ studn's. Tn general, eurr<Mil evidence on 

di\ersilication in Madiinae appears \n he c'onsistent with (dausen et ah"s views conciafhng the im[Kfrtance of ecological factors 
\\\ incipient e\ oinlionary divergence. Phylogeny of Madiinae is no longer [he intraetahle proi>lem p(M-cci\ed h) 
I'clalively little is known alxiul the hiologieal hasis foi- the exticme e\olntionar\ propen^ilies of larwecds. 

Key HonLs: Adaptive radiation. cr\ptie diversitv. di\ ersifieation. edaphic entlennsm. Holocarpha. Ijivifi, Mdd'us. 
i\ladi!nat\ ])eripheral isolates. reprodncti\e i.^olation. >pecialIou. 

' Original research [)n'senled here was supitorted l)\ the Xalioual Science Foundation (NSF-DKH 9'\\M\2'M). the Lawrence 
\\. Ileckard lMidowm<-nt Kund t>f the J(^pson llerharium, and Kodeiic H. Park and othci" genei-ons conlrihnlois lo the Ji^pson 
llerharium. Figures 1,2,6-8. 10. II. 1 1. and 1 Ti wia-e illusi raled hy the late Jeanne Janish (lettering addetlj, f|-om Ahram.-., 
Lero\ and Fen-is. ijoxana Stinchfield. Illnslmlefl Flf>ra nf the Pnnjle Sidles. Volume IV. Copyright ® l^GO Ln die Boai'd of 
frustees ol the Feland Stanfonl Jr. Fni\ easily. All riglit> n\-ei\ed. Used with ihe pcrmissioti of Stanh>r-d Fniversil\ I^ivss. 
www-.snpa>rg. Figures 19-2-1- wen^ illuMraled In l.esle\ Hamlall (lelteriiig added), and !■ igin-e 23 was lllnstralcd \)\ Karen Klitz. 

^ T T \_ _ ^ [ ______ _ 

I (hank Feler IF Ihncn for inviting me to [iarliei])ale in the Missouri Botanical (iarden's SOlli Annual S^^tematics S)mposium, 
where a version of this papei- was fii'st prcsenlcfL and Peter K. Crant. B. Bosemai) Crant. Jonathan IL I .osos. Foren 11. 
Bieseheig, Ann K, Sakai, Christopher J. Schneider. David B. W ake. and Mary I\ W insor for sharing iheir data and helpful 
insights on evohilionaiy di\(n■^ification at the symposimn. 1 also thank Jolni F. Strother for reviewing the manuscript. Bridget 
F. Wessa h.r lah assistance, Susan J. Bainhridge for field assistance. Rcxford F. Fahiii-r h.r ].!-o\ iding li\ iiig s(-cd collcctioir- t)f 
lfiiliicarp!i(t, Gerald 1). (^ari- foi- adapting Figure 3. and all Madiinae researchers, past and present, for their exten>I\e 
contrihutitms to understanding of this [a^cInalilig grou[) nf plants. 

"Jepsrtn llerharium and nepartment of Integrative Bioh»g\. 1001 \alle> Flh- Seicneo Building #2 Km. Fui\ersit\ of 
California, lierkelev. CA 94720-2 !()."). F.S.A. I )haldwinC«'h( 

AN^. Missoido l]()t. Gai^i). 9;5: 61-93. PLhiisiti-d) ox 31 Ma\ 2006 

Volume 93, Number 1 


Clausen, Keck, and Hiesey Revisited 




Contrasting modes of diversirication (specialion) presented by Clausen in his 1951 book, Avhich has 

have been suggested to explain evolulionary ehange been a major inspiration (or generations of Madiinae 
Avithin diderenl lineages of subtril)e Macbniae (Com- 

positae), a monophyletie plant group of 119 speeies Here, I revisit some of Clausen, Keek, and Hiesey's 

romnioidy known cis tanveeds (see Baldwin, 2003a). hy})otheses of evohitionaiy ehange in Madiinae and 

The name "tarweed'' belies the great morphologieal evolutionary hypotheses ol subsequent tarvveed re- 

and eeologieal breadth of plant life eneompassed by searehers who, at least in part, based their studies on 

Madiinae, especially by the Hawaiian silversword 

previous wot 

'k by 

one or more mem 



f tl 


allianee, a famous example of adaplive radiation (see Carnegie team. Addition of a molecular phylogenetic 

Bahbvin, 2003lj, c). The Californian or continental framework has proven useful for re-evaluating pre- 

tanveeds, in general, are h'ss diverse ecologically than viously suggested modes of diversilicalion in various 

tlie silversword alliance but contain about three-fold groups of Madiinae, bearing in mind the limitations of 

more recognized species and have been uiider phylogenetic data for inferring such evolutionary 

evolutionary investigation (ar longer than have the pi-()cesses (see Losos & Glor, 2003). Tn light of data 

Hawaiian taxa. A recent book, Tanveeds & Silver- from tliose recent and ongoing studies, I suggest that 

sivords: Evolution of the Madiinae (Asteraceae), the contrasls in processes of tarweetl evolution so well 

includes extensive reviews on natural history, mor- documented by Clausen, Keck, and Hiesey in 

phological and taxonomic diversity, chromosome cf)mparisons across genera are far more extensive 

evolution, hybridization, glandular structures, leal dian earlier appreciated. In addition, new molecular 

and wood anatomy, secondary diemislry, molecular perspectives demonstrate that phylogenetic structure 

evolution, conservation genetics, evolutionary rela- in Madiinae extends to finer-scale levels than 

tionships, and processes of diversification in Califor- previously suggested, in part probably reflecting 
nian and Haw'aiian Madiinae (Carlquist et al., 2003). 

The first evolutionary studies of tarweeds began at conform, at least in some measure, to Clausen et 
the Carnegie Institution of Washington at Stanford, al.'s (1939, 1940, 1948) ecotype concept. 
California, with pioneering biosystematic investiga- 
tions by Harvey Monroe Hall and E. B. Babcock on Exori tionary Contiusts ijetwekn Major Lineages 

Hemizonia DC. (Babcock & Hall, 1924) and by Qp LwiA 
Hall and his two junior colleagues David D. Ket:k 
and William M. Hiesey 

divergence of ecologically distinct lineages that 

on various lineages of 


allopalric divergence 


•n tl 

le n 


Madiinae (Hall, 1932). Hall recruit(Hl Danish plant Layia lineage. A widely studied hypothesis of 

evolutionist Jens Clausen to join the research team at diversilication in the California taj'weeds considered 

the Carnegie bistilution in 1931; Clausen assumed the by Clausen, Keck, and Hiesey concerns the group of 

position ol principal researcher four niojiths later, taxa in Layia Hook. & Arn. ex DC. with seven pairs of 

follow'ing Halbs untimely death in 1932, and piu'sued chromosomes. Members ol Layia are spring ephem- 

decades of tarweed research there as leader of the erals that sometimes have white-lipped ray corollas 

renowned Clausen, Keck, and Hiesey team (see and are commonly called "lidy-tips" (Figs. 1, 2; see 

Bahlwin, 2003b, c). Clausen et al. (1941) investigated 

part by 

French, 1989). 

Clausen, Keck, and Hiesey are best known for their the evolution of Layia extensively, in 

reciprocal transplant studies along Hall's (1932) west- examining crossability and interfertility among all 

east ecological transect of California (e.g., Clausen et members of the genus. Their crossing diagram for 

al., 1940, 1948), which helped establish the impor- Layia (Fig. 3) illustrates the intrinsic potential for 
tance of local adaptation in explaining variation in 


ne fl 


estimated from seed set and extent of 

widespread plant species. Less widely appreciated are chromosome i)airing in F] hybrids. Clausen et al. 

Clausen, Keck, and Hiesey's broader interests in (1941) regarded taxa with seven pairs of chromo- 

understandiiig how diversity arises in plants and their somes, on the lett side of the figure, as constituting 

extensive experimental studies on Californian tar- one of two "majoi- l)loeks ol species'' in Layia, which 

weeds. In his syntluvsis, Stages in the Evolution of in turn was sulxlivided into three, informal "com- 

Planl Species, Clausen (1951) showed that plant plexes," each unit(H] by morphological characteristics 

groups recognized by taxonomists as species represent and moderate levels of interfertility: (1) L. rhrysanlhe- 
a wide diversity ol evolutionary entities that can 
differ greatly in relative levels of morphological, 
ecological, and genetic divergence and can arise 

moides (DC.) A. Gray and L. frenionlii (Torr. & A. 

Gray ex A. (xray) A. Gray. (2) L. jonesii A. Gray, L. 

leucopappa D. 1). Keck, and L. munzii 1). D. Keck, and 
by distinct processes, Californian tarweeds con- (3) L. platyglossa (Fisch. & C. A. Mey.) A. Gray, 
stitute about half of the evolutionaiy examples Stebbins (1949: 232) regarded ihe interfertile taxa in 


Annals of the 

Missouri Botanical Garden 


Pigiifcs ] niK 

2. Wiflcly syiii|);itrir. ± iiilnsln i Ic inrtiilxM-s *){' Lnjia with srvcii pairs of cliionuisoiiics. I'"ii!.utv 1 (liTl). 
Ldvid rhrysanlhcmoides. — A. H^isr ii[ |ilant. — H. (iapiliih^sccncc. — ('.. Iiuoliif^ral hraci (ahaxial view). — I). Disk I'lon-L 
— E. Hrt'cptacular l)iact. Fi^uic 2 (riglit). Ijivia plulvi^ddssd, — \. Ilahit. — 1^ Ka\ floivt and enrf>l(liti<: irnolucral 
(adaxial \iru). — C. fii\o]iuial liracl (aha.xial \ifu). — 1). Disk Florcl. — K. i^i[»pLis ('Iciumts (tun finrns). 


each of [he (irsi Iwo coiiiph^xes ns ''species in tlu^ slale oullined hy Stebljiiis (1966) hy si 

snow iMii" lii'^ldy 


I heeoniiii*^. 



n^iiiced <^<^tielic siniilai'ilies in 

Slehhins (1^66) sho\vcas(Hl (daitspn. Keek, aiid 


pairvvise eoniparisons 
I lie tliHH^ subgroups r(dati\e lo f;"eneLie 

lliesey's (1911) biusyslenialie dala uii the ineniber.s (tf identiliivs wilhin each ^roup. 


(tviii uim (/ 


7 as exenij)lary of gratUial, allopahic 

A iiioleenlar [)liyiogerielie perspe(li\e on di\ersifi- 

rliverg(MK-e (see also Stebbiiis, 19o2). Slebl)ins (1966) eatioii of the n 

7 ineinbeis o( Layui based on 

noted lliat la\a of fjiyia vvilli moderate iiilerh'riibly nnelear ribosotna! DNA (iDNA) iiiUM'nal I tanseribcMl 

are Invatiabl} alloj^atrie; iti eonlrast, la\a that are 

s)nipal.rie are nKjJeratelx lo highK' intersleiile, with 

s[)aeer (ITS) sequences (Fig. 5; liaJtlw in, 2003a. 
unpublished) reinforces the e\"o]ntioTiarv con(dusions 

reduced ehroniosome pairing at UKMotie nu4aphase T of Clauseu el al. (1911), Stebbins (1966), ai 
in Fi h>brids (Fig. 4). Under llie assuniplion that Waru ick and (n)lllieb (]9o5). Mono[iliyl\ of ih(w; 


degree ol niter(<nliH[y rellecis recency of common 


group is Avell snj^porlcd, as are each of the unce 



anceslr) (a ilsky premise; see Donoghue, DJIir)), (he snbgr(»nps ("coniplcxi^s") jiropostxl by (Clausen et al. 

patlei'ns sh(t\vn in Fi 

a' 1 1 re 

1- arc consistent \\]\\] ihe (1911). 'Hie tree le[K)logy afid branch-lengths corre- 

hypothesis that s}inpatric- taxa undci'wcnl carluM- Sjxjud u(dl iu Clausen el al.V (1941) modtd of gradual, 
divergence from a connnon auccstoi" comj)ar<Ml lo allopalric (h\ ersificabon, with svmpatric 

!a\a being 

alloj)alric taxa or populations in each of [he llu'ce d(^(-ply (h\(M-gent relative to allopali-ic members of 
suI)groups, and that sympatry is secondary, followiii 




eacn snhgi-ou[) and i\\ c<tmparison 
the (// = o) siste]'-gj"onj) lo the n - 

to b 

n(vnres ni 


a period of lineage di\ej"genc<' \i\ geographic isolalion. 

\\ar^vick and Gotllieb (DXio) re-e\aniin<'(l the results piovide no evidence of accelerated I 

hypothesis of g|-adnal. alhjpalric divergence among inlerfeililitv within aii\ ])ar! of the n ~ 1 


incage. The 

uss o 



w n 

7 mcmlx-rs o( L(iyi({ from the perspective of wherein inlernal barrier^ lo gene flow niav well reflect 

the fnidiugs of byf^roducls of gradual (nolntionary (Hxcrg^Mice. Not 

shown in Figure 5 \^ the finding (Haldw in, un- 

allozvnies. Their results mirrored 

Clausen, Keck, and lliesey (1941) and the scenai'io 

Volume 93, Number 1 


Clausen, Keck, and Hiesey Revisited 


^ 4 « 4. ri ri V 

k * i i I 

* * 

^ <y} H I M iT x 

* • • ****//, , 

. . .vXv:':-:^-:::::::^;::-:-:-::;-:'::::;-:-^- ■• 

• ,^1**-.- ■ ' ■ • V ,-,,- *<-» 

' • * ' ■ \\\\\\\,\ *'*" ' 

» * /, ,,.--- . - - > 1 

' '■-*--, , . ,, 

J 4 




^S^^ liliiii glandulosa 

# 4 t 

4 * 

^1 * t 

* ■ 

+ 4 ^ * 

4 » ■ « 

i * * * • ■ 





fe • ■ 

§ It />:#■■■-■'••:■: pentachaeta 

■ ■ * 

r* -* 

t 4 

W i 

L*/,** 4 4 t ■ ■ » ij 

I * ^1 

, fr * 

f t 

4 * « ^ 

t ^ * 4 P 



+ **■■*• 

4 ri ■ 



■ ^ ^ ^ — 


t 1 

■ n 

4 *i 

V 4 

-. *4-»*4t-P'""* 


* •/ 

, , , , • Ji ■ * * t - * * * ' -^ - " 

N ^ * 

4 * *_ 

4 « 

4 4 ■ 4 

n=8 ): hieracioides 




4 ^ 


\ < 

1 4 

L+ * 

\i ^♦-*4 *X_j( 

f T ' 

* » * T 

4 ■ 

h ■ P * » * • ^ 
1 i4«r«4* 

4 4 > 4 P 

f ^ * 4 4 

i « 

■ * ^ P * ^ * 
» , 4 4 » 4 4 ^ 

• 4 ■ * * * *■ 


» 4 

t ^ ^ 

1 * 

i 1 * 1 ^ ■■ ' * » 


'?>^::o;-^ n=fi 1-:' 


^^§. heterotricha 

Figure 3. Crossing diagram oUjtyia, adapted from Clausen. Keck, and Hiesey (1911). Cin-h.^s represent different spe(;icri; 
siz(! of circles roughly illustrates relative alnindancc of each species, '\^^i<hh of shaded connections between species indicates 
estimated intrinsic potential for gene flow ])ased on seed set in F| h} brids. Width of lines connecting species indicates degree 
of chromosome pairing at meiotic mctaphase 1 in Vi hyf)riffs; nunii)er(s) of rneiotic chromosome pairs in F] hybrids or 
vegetative condition of non-flowering hybrids are presented ahmg lines. Dotted lines between species or groups ol species 
indicate major discontinuities in morphological variation. Used by pc^-rnission of the publisher, Carnegie Institution 
of Washington. 

published) that rDNA sequences from differenL oflf-n vergence of chciiacleristics across lineages present 

widely separated populations of each species were minimal problems for systetnatists; even application of 

resolved within a common, tiionophyletic lineage, as phenetie criteria should provid(^ accurate reconstruc- 

expected under Clausen et al.'s (1941) evolutionary lions of relationships under such conditions (see 




re n 

7 lineage of Layia evidently conforms to 

Felsenstein, 2004). These attrihnb^s are pulatively 
reflected by congruence between Clausen et al.'s 

Clausen's view of the "'most normal pattern of (1941) phylogenetic hypotheses for the n — 1 Jjiyia 

speciation," with "a more or 



s snnuttaneous an 


group (based on essentially phenetie considerations of 
gradual separation in morphologic, eeologic, genetic, morphological similarity, chromosome-numljer simi- 
and cytologic characteristics" (Clausen, 1951: 90). larity, and levels of meiotic chromosome pairing and 
Groups that exhibit approximately rate-constant di- interfertillty) and clades resolved frotn molecular 


Annals of the 

Missouri Botanical Garden 

Distribution and interfertility of six species of Layiq 

Data from J. Clausen, 1951 

L chrysantfiemoides 
L fremontii 

L. }onesii/ L munzii 

L. leucopappo 

L platyglossa 

Meiotic pairing, F^ hybrid = 711 Fertility 25-30% 

Melotic poiring, F^ hybrid = 5-711 Fertility 5-20% 
Meiotic poiring, F, hybrid = 2-611 Fertility 0.5-2% 

Figure 1. I)islrii>uli(>ns iitul inl(M-iri-Iilitios of spocirs of/.f/v/*/ wilh sovrn p.iirr^ of cliromnsomcs. Ix-tters aloiig.sidc specie.-^ 
(Il.-lnlnilioiis tMin-f'spinid hi llic firsl l('t[ri(^j in spfH'i(^s fpillid of iliosc la\a (C = A. chrvsunllirninidrs: V = L. frcnio/iiil: J = L 
joncsii] I. = /.. IciicufKjppd; M = L. nutuzil: I'l = !.. I'lah^lnssn). \(»te niodcraU' lo lii,iili inlci-ffitilih ofniosl ^illopalri)- sprcirs 
and low iiilrrf<'rl dity ofwidtd) .sMiipalric sprcirs. Iicpriiilcd Ir^Jiii Stchhitis (l'X)(>), h) pormissi(Mi of Trarsoii Fdu( ;ilit>iK Uppor 
Saddio l>i\c!\ \\r\\ Jorscv. 

j)h\lt»*!:eiietic atuiIy.M:s. As iioltal alioxr. llir three n — 
7 "spcci(^s complexes" [H'oposed I))' (Clausen et al. 
(1941) ('()rr(^si)oiid prceiscdy to clades I -.'5 iti Kliiure S; all 

in addition, Clausen fl9o 

29-130) indicated that 

"Ixiyia pldfyglossd is almost a s|)ecie^ eomph^x in 

Accelerafi'd phenohpu: (hier^ence iit n 

- 8 

r.ayia hncdi^rs. In coiiliasl to evideiua^ for ^ratlual. 


opalric <livei'getiee in llie // 

7 Ldvid lineaii;e. 

(^\]}erimenlal and molecular data from tlie congeneric- 


8 sistei-lineage luuc re\'ea1ed nudlipl(^ examjtles 

iisell. . . Tl is genelieally sliar[>ly sejiarated Irom of iaxa thai Hktdv arose 



in [>eriph<a'al or 

(■lirysan(li(>m<)i(lrs and Frcmonlii and... is more elose- 
]y related. . . to. . . Icucopappd^ Munzii, and ]()iiesii\ in 
ei)m])hMe eonloiinily with the rl)NA tice lopolog\ 
(Figure ,')). 





eeolo'i,icalh (list met stUhntis. 


lylogenelK- and phenoiypie palterns am 

- [] suhli 

liming of 

n cages are 

diwrsiliealion resol\etl In two /? — 

sirTiihu". a I least in pai t. to (^xpeeterl outcomes of 

Volume 93, Number 1 


Clausen, Keck, and Hiesey Revisited 


n = 7 


2-6 11 

L glandulosa/discoidea 

L gaillardioides & relatives 

8 11 Lh 
0-5 II Lc 




<80% bootstrap 

>80-90% bootstrap 
>90% bootstrap 


L platyglossa 
L platyglossa 

L platyglossa 
L platyglossa 

L jonesii 

L munzii 

L leucopappa 

L chrysanthemoides 
L chrysanthemoides 

L fremontii 

L fremontii 

L glandulosa 
L glandulosa 

L disco idea 

L pentachaeta 
L pentachaeta 

L gaillardioides 
L gaillardioides 

L hieracioides 

L hieracioides 

L. carnosa 

L carnosa 

L carnosa 

L septentrionalis 
L septentrionalis 

L heterotricha 

0.005 substitutions/site 

L. heterotricha 

Vl^uvc 7). 

(IJalduiii, 2(.)0*ku uiipiilili.-li«-(ij; nnr of two maximally parsimonious Irces (■•• 

Plnlo^eiu'tlf li)i)(j[lu>is [uv Lnyia based on nuclrar 18S-2()S rDNA inlcnud IninsrrilxHl spnrrr sequences 

= clade uni'esoKed in sliiel eon^t^n&us Iree). 

Hrani-li l<'n"-dis eorrespond lo n'lati\e time since divtn-geiice, nnd<M- maximum-likelihood oplimi/alion: lale eon>lanc\ ol IIS 
e\i)lnlii.u a<Toss lineages eoultl nol lie rejceled uslnp; FelseiL^Lein's (1988) likelihood-ralio lesl. In die /J = 7 group, elades lA, 
2A. and :]\ re[)resent Clausen el al/s (19 I Ij llnee "complexes" ofalKipalric species, discussed in die lexl. Numbers of meiotie 
eliromosonie pairs in F| li)l)iids jn-lueen ta\a in a clade are indicated ahovt^ hi-anclies (Lh = hybrid uilh (hphud L 
hicnicioldrs: Lc = hybrid uidi L. nirnosd; Ml = no hybrids reported), Ijaseil on Clauhcii el al/s (1911) crossing data Un- Layia 
(se(^ Kig. ;^). The tree was rooled usin^- Arnica mollis TTook., tlulsea al^ida A. Gray, RaiUardvUa pringld Creene, and 
[dcnofhainitiLS validus (Ki'audc'^ce) I). I). Keck as the oulgrou]). Terminal taxa of die same name re])i-esenl geogra[)hieally 


disiunci populations. See Appondix 1 U)\- aiit[i(trship of species names nol mentioned in lexl. 


Annals of the 

Missouri Botanical Garden 


L<i]it! discd'uh'd. — A. Ihiiiil. — H. 
Fi^iin- 7 (li^lil). Ijiy'in i^lainhdnsa 
(Lilrca! \ lew). 

} (li^liiict. itihM-frrlilf liictiihcrs n\' La)i(i uilh cinhi pairs of chnniHj.sotucs. Flguif 6 (left). 
I'l-iiit with pappus. — (.:. I\i[)])ns ('icniiMil (al)n\i;il \ir\\). — D. Pappii> (^Icinciil (lateral \\c\\). 
— A. Ifabil (hisected). — ^I^, Involiii-ial l»ra(l. — C. ImiiM \vt|[i jvt[)piis. — 1). l'ap[)tis rlciiicnl 

peripalric s])criali()ii (Ma) i\ 19o2), quaiilum (-volulion examples of species pairs ifi plauls thai represent 
(Slinpsoiu 1944). (ir (jiiariUun sp(H'ialion (Grant, 1063, ])nlative (waniples of lineages wherein one species 

1971; Lewis, 1966), as discussed lj(d()w. 


F^nhit KMiary (n\('r^enee 



a locat geo^^i-aphie 

d('seend(ul froiii ancestors in another; he dis 
e\idenee lor l>nd(hng-orf of three annual diploid 

scale m general has l)e(M] widtdy suggeslc-d to he of s|)(H-it;> of angiospenns, including an // 
major importance ifi plant evohilion (e.g.. Ehrlieli & of Ijiyia, L. discoiflra D. D. Keek. 

8 n 



d he hest-stiahed hypothesis of rapid evolution 

leaven, I ')(>*); I.e\in, 1. 993), allhougli con\iiieIng 
pliylogenelie evifleiice for a putati\ely common 
pattern (tf local di\('rsifieation, i.e., 'Inidding off of L disandni (Fiu. 6). which is moriiliologicallv 

amonii tlie // 


o Ijiym laxa eoncenis the origin of 


ih.>luieti\e. new 

incages Irom within a ielati\elv unusual that it was not iniliallv nxQo-nized to he 

(uiilorm set of r(da((Ml Hneaires. i; 

_, , . .s nsiiaii\ 


acKuig ui 

a larwccti — and was ahoul to be deseril 



studies of suspected "|>i-ogenIlor-derivative*" species a monot\pic 



"if)\] r 

a." f 

or eo-(hseoverers 

pairs (see (;ollhel), 2()0lj. Fxpected ])arai)hyly of Roxana S. Ferris and Ira L. Wiggins)— until Clausen 

a wid(^spread "[)rog(autor" s])eeies relative to a "de- e[ ah (1911) observed some similarities with larweeds 

rivati\e" isolate iii sonu' models of local dixersifica- and suhsequenti) found that the plant was com[)Iet(dy 

tion may (ad U) he resolved in pliylogenetic anal}ses iuterrertlle with /.. gLuuliilosn (Hook.) flook. & Arn. 

heeause of insufricicullv hioh nilcs nf Pvnliuinn in (f^ig. 7). Despite being fully interfertiie, L ^'7a/k////fwa 

because ol insud'ieiiattly high rales of evo]uti(m in 


I L 

(liscoidca dider gi'eatly in inor[)hology and 

(lie (diaracters under study, extinction or inadequate 
sampling of popidaii.)ns (see Neigel & Avise, 19C6), ecoh)gy. For example, like most tarweeds, L glandu- 
or gcaie flow among lineages within the paraphyl(^tic lo.ui has ray fhuvts and iuvolueral bracts; I. disvoidca 
])rogeuitor laxon ((\g., for genes under strong lacks bo[h ray florets and true iuvolueral bracts, with 
selection; see Kieseberg & Burke. 2()()1). Rased on marginal reeepta(adar bracts constituting a false in- 
various theoretical considerations, Rieseberg & volucre. 1die two laxa also differ substantiallv in 


Bruuillet (1991) suggested that paraphviv of plant h-atiu-cs of the pappus. Layid gUindulosa occurs 

species ma_\ be common. Cottlieb (2001) li->t(nl .'51 mosll) In coars(^ saiidv soils, iiududim.^ sand dunes. 

Volume 93, Number 1 


Clausen, Keck, and Hiesey Revisited 


111 s(Miii-ari(l and montane rcginns of California and llie 
\vest(^rn deserts; I., dandulosa has the widest 

the Ivvo phenol) pieally dissimilar taxa consliliile 

a n 




. Si 

long support 

for the nested 

within J., ghnidiilosa 

(see Baldwin, 2003h, e). f.ayi(i disroidea is confined to 

dislrihntion of anv ohlii^ale outerosser in Madiinae placement of L discoidca 

_r \- -r 

corrol)orates Gottlieb el al/s (1985) hypotliesis thai 

seri»enlinc barrens in a small region of thelnner South L discoidca descended from a lineage of A. gJandii- 

Coast Ranges of California (San Benito and weslern losa. Gottlieb el al/s (1985) ad(htional conclusion [hat 

Fresno counties). Serpentine (M'odes to clay (siructnr- L disroidea represents an example of relatively recent 

all) unlike the sandy habilals of L glandulosa), has evolution is also evident from the ITS tree; the branch 

a high magnesium/calcium ratio unfavorable for mosi separating L discoidca from the most closely related 

plants, is low in some essential plant nutrients, and iin(^age oft. glandulosa in the rate-conslani TPS tree 

contains concentrations of heavy metals that can be is comparable or shorter iti length to brandies of 

loxie to angiosperms (see Kruckeberg, 2002), Ap- conspecific sequences in other members of Layia. 

proximalcly 9% of minimal-rank vascular [)hml e.g.. L pcniachacia A. Gray, the sister-species lo L 
taxa (si)ecies, subspecit^s, and varieties) endenu'c to 
the California Fh:)riftlic Province are confined to 

glandidosa anrl L discoidca. 

A more extensive |)h) h>g(au^tic analysis of relation- 
seri)enlin(^s (Kruckeberg, 1992) and have Ix^en ships within the Layia glandulosa/L discoidca lineage 
interpreted either as pr(Khicts of recent, /// sila bascn] on ex[)and(Hl sampling of populations and 

volulionary relicts s(Hiuences, with combincnl ITS and ETS (exlernal 

evolution (neoendemics) or as e\ 
(paleocndemics) thai beeanu- secondarily restricted to transcribed spacer) data, yielded a nearly noise-free 
serpentine habitats, possibly by comi)etition or in- tree that reinforct^s su[)|Ktrt for recent descent of L 
lerference with other taxa, in association witli kite r//.sro/V/ea from a sublineage of L g'/a/?r//// (IJaldwm, 
Cen(»zoic climatic changes (see Raven & Axelrod. 200.5), Sequences of the five populations of L. 

discoidca sampled are identical; sequences of L 


Ldandulosa are helerog(aieous and are resoUed as 

On ihe basis of morphological and ecologiral 
considcTations, Clausen (1951: 82) conchided thai a grade of lineages that are geographically distinct 
Layia discoidca was "|>'"*'1>^'l>ly an eda])hic race (of L and, to some extent, morphologically divctgenl. For 
glandulosa) adapted to the serpentine soil, and -v.,muJ.^ tl,^ ^UuM-un.Mn lo all other lineao:es m the L 
possibly an ancient relict." Clausen et al. (1947: 
121) were unable to resoUe the rclalionslui) belwei'u 
the two taxa: 'There is no way of determining which sand dunes. Phenoly|>ic dls[)arity among the lineages 
rat-e uas first, the rare, ineonspicuous one from the of L glandulosa is minimah how(w-er, compan^d to 

e\ami>le, Uie sisler-gr(ui[> to all other lineages in the 
i>Iandiilosa/L discoidca clade is a inor[)holngicall) 


ana ecoio"; 

logically discrete group end(M7iic to coastal 

serpentine (L discoidca), or the common, show^y one 
from sandv habitats (/.. glandulosa),'' 

uunphological and eeologieal differences between L 
discoidca and relaliv(^s in L glandulosa. Fine-scale 
In the 198()s, Gottlieb and enlleagues revisited ihe |)atterns resolved in die ETS+ITS tree are consistent 
orioin and age of Layia discoidca. Gottlieb et al. with Ford and Gollbedrs (1990) conclusion that 
(1985) found that genetic similarity belwecn L yellow-rayed populations of L glandulosa, sometimes 

treated as L. glandulosa suljsp. lutea D. IJ. Kec:k, are 
tlie cdosest relatives of /.. discoidca, which lacks ray 
floret:^ but has one or more modifier gene(s) for y(dlow 

discoidca and L glandulosa, based on allozymcs, 
was almost as higli as values t\pical of conspecific 
iilanl populations. They conchuh-d thai the ser|)enlinc 


/.. discoid 

iscoidca represents an ex 

:ample of ray-corolla color: most j)opulations of /.. glandulosa 

a peripheral isolate that diverged relatively rapidly have white ray corollas and all but one of the sampled 
and recently in an ecologically marginal setting from while-rayed populations arc resolved, based on the 

an ancestor referable to the geograpliically widespn^id 
L glandulosa. Ford and (ioltlleb (1989, 1990) 

molecular data, as more distantly related lo L 
discoidca than are the sampled yellow-rayed popula- 

corroborated Clausen et al.'s (1917) conclusion ihal lions. 

only two major genes are responsible for pi'estmce oi 

As noted by Gotlhcb (200 !), the evolulionaiy origin 

absence of j-av florets and associated involucral bracts of Liyia discoidca did nol iiuolve the major gen()ty])ic 

effects predicted under quantum speclation (Cirant, 

in L. glandulosa and L. discoidca and show^ed that 

mor[)hological differences biitween llie two taxa are 1981); compleU^ inlerfertility with L glandulosa and 

controlled by "a comph-x admixture of genes 



the higlily contrasting edaphic settings of the two taxa 

large and small, qualitative and (luantitative effects" implicate ecological selection without radical genetic 
(Ford & Gottlieb, 1990: 44). 

reorganization in di\crgence of L. discoidca, in 
keeping with some reeenl. general vi(wvs on acceler- 

Tn the ITS trees for Layia (Fig. 5), resolution of 
a clade comprising L discoidca and L glandulosa ated evolution in i)cripheral populations (e.g., liarlon 
corroborates Clausen et al.'s (1947) hypothesis thai & Charlesw^orth, 198 I; Coyne, 1994). Alayr's (1982: 5) 


Annals of the 

Missouri Botanical Garden 

Kijiiire 8. 

Layia galUiudioldes (u = 11). ^\. S\vm scgnu-jil. 

H. Capiliilcscrncp. uilli |)c(]miclf' dclail. — (]. I 

ti\ (►liirr 

a I 

bract fahaxial ^u■^^].—D. Iiuolurrai l.ra.l ( lateral viru). _E. Ka) Hun-l (a.Jaxlah i<'u). — F. Disk fkavl. — C. Pa|)|,ii. ('Irnicnl 

(lateral \ irw). 

reliiKMiient of \u> cavllvi ideas on rapid diver-ciicc uf ClauseiiV (19.11) sng-oslioii diat west-east iiilerpop- 
|)erl|.Iieral isolates or foiinders n.eripatrie speeia- ulatioiia! diHereiK-es in /. gaillardioidcs reHeel 

^(Mielie divergeiiee, ihongli al a dee])er (^\ olulionaiy 

n lie proposed. Four major, allopalrie 

lioiT') allowed (or tlu^ possihilil) of ''rapid eliaiij^e. . . 


more to greatlv increased selection 

J ires 

1 tJK 

>ures. . . than lo [I 

le genet le 






etoser cU:eor( 


eoiise([Lienet^s of in- evolnlionar) IiiH«ages uidiiti A. gmllardio'ulcs are well 
vvitli the pro|)os(Ml supported l)y rl)\A data and three of the fom- lineages 

evolutionary scenario for /. disroidra. Proximity of rejilaee one another from west t(. east thron-h [hi 
potential hahilat.^ of L gUnidulosn and L discnidcd 
even ]ea\es open (he [)ossihility llial diverg(MU-e of A. 

(^oasl Rangers (F>ald\\iii, nnpuljli>hed). 

Ihe four serni-cr\|>lic, allopalrie lineages of Ijiyia 
disroidea nu.y have (.eeurred in die presene(; of ^^r/^7A//Y//o/r/e^ (!(> tuU (-(mslitute a ('latl^' iii rl)N A 
|)oleullal for gene flow with /.. p:huidid()S(K altltcaio;h 


adjacency of populations of the two taxa has nol heen 
documeuled and iio eviden(;e of hvhridi/atiot 
apparfMit from the rI)[N A se(|nences. 

morphologically and ecological I v (h'stiiicl L. 





cuniosd (Nutt.j Torr. <S: A. Cra\, L hi 

(l)(^.) lloolv. iK Arn., atid L si'iilcntrioiiidis D. I). 

Keek are nested among llneag(^s of L gadlardioides 

A less widciv studied example (.r rapid evolutionary and ap|)ear to repres(ail example^ of accelerated 

enange among the // 

= 8 Ijiyiit taxa concerns L. 
gdlllardioidrs (Hook. & Arn.) DC. (Fig. 8) and eh)se 
jelati\'es. Clausen (1931: l()j regarded tlie extensi\(; 
intetpojndational variation in ray corolla e(tlor, 
vegetative mnri)hology, and floweritig time ^vithin /.. 
gdillnrdioidcs as "vei"}^ spi'ctacular.'" In |)arl hased ou 
e(Mmiion-garden studies, he eotielnded that soti^e 
vai-iation among [)(>pu hit ions of /.. gaillardloides. 

phenotypie (hvei-gence froin /.. ^>7//7/r//7//o/V/e,s-like 
an<'estors (15a hi win, uii])[il}lishe(h Fig. o includes 
r(^pieseiital!\es of IJirt^e of ihe four major litieages of 
A. gfuUardioidcs). Layia (■(irnosd (Fig. 10), a rare 
etuh'mie o( ouU'r coastal foredmies, o(.:cu[Mes a mar- 

e.g., in leaf margins (Fig. 9), is heritahh; and htllovvs 
a wesl-easi g(^ographic ])atter]i ^'correlated 

ginal ecological setting where . ,. ^ 

uot occur. A h}podiesis that L. 

a peripheial isolate at the eoa<tal-most I inn Is of 

/-. i'ddldrditfidrs does 

(■(irnosa arose as 


a \vid(^spr<\id jirogenilor is cousisleiit will) distiihu- 
lious of the h\o closest relalives of ^'heaeh layia'': 
ecological differences helween ihe outer and inner (I) a lineage of L gaillardioidcs that occurs along 
Coast Range" (Clausen, 19.31: FI-15). Phylogenetic winduard slopes of die Norlh CoasI Ranges and San 
anal)'sis of rONA stMjucnces of Layia corrohorates 



Francisco Hay Area and (2) L liirniciaidcs (Fig. 11), 

Volume 93, Number 1 


Clausen, Keck, and Hiesey Revisited 










9. Basal-lraf variatioti \vitliin and among si\ pnjHiiations o( Lavia gailhtnlioidcs. Karli leaf represents a dilferenl 

itions at Stanford. Three populations from llie ouler Coast Ranges of California 

ni(li\iinial "ironri under eoninion 



en eoiK 

are re[)resenled at left; three populalions from the Inner Coast Ranges of California are represented at right (lop-to-hoKoni 
equates to norlli-lo-soulh distrlhution of |)opulalions). Note deeper ]eaf-l(»hing in populations from the dv'wv, hotter inU^ior of 
the state. Repiinled from Sniges in the Krolul'um of ritint Species, ]^\ Jens Chnisen. (^opyriglil ® 1951 In Cornell Univei'sily. 
Used hy p(M-mission of the publisher, Cornell Univ. Piess. 

wliich occurs widely in the Stuilli Coast Ranges, in rDNA trees (JMg. 5), is an ohligately oulcrossing, 

part on sandy soils and even coastal hackdtmes. Self- narrowly dislrihuted plant of poor, sandy or serpentine 

eonipatiltility in L caniosa and L hicracioldes soils that oecin-s in interior regions of the North (j)ast 

(Claus(Mi, 19ol) — otherwise unknown In Layia — is Ranges, wliere population^ of one major lineage of L. 

conspicuous morphological gaillardioides occur sporadically: the two taxa have 





1 some 

diHcrcticc^s from other members of llie L gaillar- not been reported to occur together. 

dioides cladc (e.g., reduced sizes of ray corollas and 

Parallels l)etween patterns of evolutionary change 

heads). The putative shift toward a more highly in the L guilUirdioidcs assemblage and the L, 

glandiilos(i/L. discoidea lineage, discussed above, do 

inhrceding mating system in the sel(-cotnpald)Ie taxa 

be reasonably suspected to ha\(' [)romoled not extend to patt(M-ns of interfertility. In contrast lo 
evobitionarv (diange, as suggested by Gottlieb (1973) complete inlerfei llllty between members ol L ghm- 


w * 

(jr origui o 

f tl 


771(11 ncumisis 

le seif-compatibh; Slrphiif}077}cria dulosa and L discoidra., members of L gdilUu-dioldcs 
Gottlieb (Cichorieae; Com|)ositae), are largely to completely intersterile with meml>ers o( 

a w(dl-sttidicd example of local, raj)i<l phenotypic L crmiosa and L. srpte}}i7ioi\alis and are largely 

divergence from self-inct)mpalll>le ancestors (see interfertile with dijiloid members of L hieracioides 

Cottli<'l). 2004). Liyia sepKvUriondlls, the other laxon (Fig. 3; Clausen, 1951; Baldwin, unpublished). 

n(^stfHl among lineages of L g<iiU(i7-dioidcs in the Consideration of tlu; observed interfertilitv jiatU'i-ns 


Annals of the 

Missouri Botanical Garden 

1^ i<:;iiri's 

A. I];ihil. 


It' iiiid 11. S(~ir-('nfiipalil)lc Iii\a In Ijnid uilh r\'^\\[ pairs of cliiOMiosotiirs. Yh^uvv 10 
— li. Involucral brad (ahaxial view). 

il (ti;;lil). fjiMf! Iiirrarioides. — 

C, Ray llincl (adaxial \ icu 

D, l)l^k lluivL 

A. Proximal -^tcrii. lra\"es. am! ['oftls. 

cnldliling Iinolucral hrai I (ailaxial \i('\\). — D. Iii\ iiliicial Inad (ahaxial view). 

lifl ). Layid cdrnosa. 
-K. Pappu.-^ (.'leiiu'til. 
— C. Ra\ llnrti ami 

-B. Capiltil(*s('('n('(\ — 

K. Disk floret. — 1"'. Pappus elrtn<Mil. 


\c fi 

8 Lnyiii cladc' CMroinpassiiiii; A. a-hindn- 

lli(^ pa[ap)i\ Idle L. gaillar- 



(1)1(1 as ail 

in a p1iy1og(MH^tic conlcxl leads iik^ to concliule lluil /.. 

c(inu)S(i and J.. scj)(i'!ilr{i>H{i!is LindeiwenI ae('el(M-ale{l losalL. discouli'ii and 

evolution of inlriusie, posl-niating i\-produdi\(' har- diuidcs and relatives stands oul 

rlers, as e\|)eeLed widi fpianUim .speeiatioii ((iraiit. excepllonal example tjf how le\els of interferlilily or 

19il), allhnngh no e\ idence of ehroniosonie repat- morpholngieal diNergenee ean he impleading alxuii 

lerning has hecu (IcUx-IchI in Lay'ia (Clauseiu 1931). 

ph)h)geny. nnlike in the n 

7 Lavia clad^N where an 

nnlike in sneh well-sludied, plant examples of (fuan- eviderilly dilTta-enl mode of e\oiulionarv divergenee 
Inm specialion as (iLirLui lingulala Harlan Lewis & led lo eongriieiil patterns of inUuferlilily, morpholog- 
M. Lewis (Lewis c'v Koherls. 1956: see (w)tt lieh, 200 I) ieal siniilarlly. and relalionshi]). Wlielher such sLuk 
and Stephanomcria uudhcureiisis (Cotdieh, 1973,^ between die n — 1 and // = 8 sister lineages 
200 I). Clausen (1 9.i 1 : 1 'M)) eonelnded that A. cdrnosd in pailerns of e\ olullonarv ehange ai'e aUrlhutahle to 
and /.. srpfcn/riofudis each reiiiesents a "nu)not\i)ie inlrinsie or exli-insic fac-tors in tli(^ Inslory of the two 
speeles eompK-x," largel\ based on inlerslerdily or groups reniains unknown. The [)rinei[)al eonelnsion 
lack of erossabdily with other la\ ias. In adchlion, that has (Miierged from nK>leenlar pliylogenelie re- 

seareli previewed here is dial evohitionajy pnx^esses 
in IjijKi have ht^en more dynamic than was (^\ident 

Clausen et al. (1911) regarded L cantosa as Inghlv 



nioiphologieally from other species or 

groups of s[)eeies in lAiyia (Pig. 3). 'Hie major l>ased (tn Clausen et al.'s (1911) bios>slenialic dat; 

niorphologleal discontinuity between A. (■(trnosd and alon(\ Evidence for multi[)le instanecxs of accelerated 

other members o{ Ijiyin percei\ed b)' Clausen. Keck. phenot)pie {n\('rgence in Iaiv'ki underscores llu; 

and lliese) now appears to refle^'l acc(derated potential importance of [)eriplierall\ isolated p(»pnla- 

inotphological evolution in /.. rarnosd, as docunuailed tiotis in plant evolution (see Ki{^sel)erg & Brouillel, 

ill the origin of/., disroidea (Lord 6L (;oltl!(d». 1990), J99k Colllleb, 2001). For syst<Mnalists, the possibilily 

I'ather than a (hsiaiil (n'olulionary ixdationship \\\\\^ that diversification is oft<'n marked b) major changes 

other members of the sanu' aenus. 

in rates ui phenolypie evolution and rates of decay of 

Volume 93, Number 1 


Clausen, Keck, and Hiesey Revisited 



interferlility across lineages, as inferred for the genelically sharply sepaialed from ils neighbors, 
principal n ^ <i Layia clade, makes risky a relianee Hybrids between members of//, rirgdia (Fig. 14) and 
on phenetic considerations for estimating relation- a rare species, //. ///ar/'ar/e/^/Vi (DC.) (ireene (Kig. 15), 
ships or circumscribing taxa, as noted earlier (e.g., exhibited iiiodesi [(Utility, in contrast to Inltastcrilil) 

between members of (hffcient ''coiispecific"' popula- 
tions of //. virgain. Palmer (1982) conducted adth- 
tional cytogenetic and niorpholf)gical studies in 
Ilolocarpha that extended Ckuisen's (1951) charac- 
terization of patterns of interlerlllity and cln-omosomal 
evolution in the e:enus. 

Donoghue, 1985). 

CiniMic Biological SPFx:n-:s ajM) Mwni) Pmcnotyimc 


As noted by Clausen (1951: 94): 'There is one 
genus of the tarweeds of California which differs 





ongouig molecular [)hylogenetic 


slndv of 

divergence in conspicuous morphological and ecolog- 

slrikingly from the pattern of specialion in Layia of Ilolocarpha (Bakh\in, unpublished) has revealed 
tlie same subtribe of the Compositae in that it has veiT evideMice of a discounc^-liim between ev(»]uliouarv 

strong barriers of sterilitv even between neighboring 
populations of one species. These populations are so 
similar in external appearance that they cannot be 
dislinguish(Mk This genus is Holocarplia."' Ilolocarpha snp[)orttxl rDXA trees based on ITS and KTS 

ical characteristics and the oiigiu of inlrinsic, post- 

mat uig reproduclive barriers iti the grou[). Well- 





Greene also differs greatly from L^j/V/ in ecology. For sequences have confirmed that each of die 
example, members of Layia escape summer dr(Highl widespread species recogni/ed b\ Clausen, Keck, and 


1 f ri I i t i 

b) tiowering and Iruitmg clunng tne wet sj^rmg 



Hiesev. i.e., //. hccrmafinii. II. ohconica (J. C. Ckuisen 
months; most members o{ Ilolocarpha tcjlerale summer & U. D. Keck) D. D. Keck, and H. rirgata, descended 

drought and (lower in summer and fall (see Baldwin 
2003b, c). 

f]-om distinct ancestors; tlu; rare fl. rfiacradatia 
descended fi'oiu an ancestor wilhin (jKU-apliyletic) H. 

timing of evolulionaiy clianges in Ilolocarpha aic now 
po^si])le because of minimal noise in the molecular 

Clausen (1951) emphasized that reproductive iso- virgaia (Fig. 16). Detaih;d conii)arisons of llic relative 
lation in plants can l)e ac-hieved by different means. 
He provifled examples of ''groups having predomi- 
nantlv ecological barriers'' (e.g.. physiological/habitat dataset. phylogenelic structure both among and within 

differences), "predominanlly mor[)liological dilleren- 

tiation" (e.g., in floral features associated wilh conslanc) 

recognizetl species, and inability to rejecl rale 

of molecular evolullcju across lineages 

pollination), and ''predominantly genetic 


t ' rs 

(Clausen, 19ol: 90-10 i) in opposition to "[uore 
tvpical s[)ecies" wherein '4he pattern (jf develoj)- 

using FelsensteinV (1988) likeh"hood-ialio lest. 

Based on braiu h-lcngth comparisons across the 
rate-constant rDNA trees, diveriience of the hiirhlv 

menl...froni ecological races is through small steps di^linctive Jlolocarplia niacradeuia Irom an anc(^sior 

invoKing the genetic and chiomosome systems and withui H. nr^ata was more recent lliati e\olnlionarv 

the morphological characters" (Clausen. 1951: 107V 

Clausens (1951) main example of diversification uitlnn H. virgata (Fig. 16: Baldwin, unpublished). 

divergence of some cry[)tic. Interslerue 

lie lineages 

dominated by the e\olution of genetic barriers to 
gene flow across lineages was Holocarpha, a tarwced 
genus with four taxonomic sj)ecies (recognl/ed on the 
basis of morphological characteristics and chromo- 
some numbers) and an indefinite number of inv 
recognized. crvptic biological species. 

Clausen, Keck, and Hiesey's experimental studies 


Ivccent origin of //. inacradenia is cousisttail wi 
modest ifilerfertilitv between //, ntacradaiia and some 


lations of H. ririxata. in contrast U^ strong 

inlcrsterilil\ barriers between most studied [)o[>ula- 
tions of//, iirgala (Clausen. 1951; Palmer. 1982). In 

ktirical e\'ohi- 

ano ecoKttr 

short, (^xlensive morphological and 

tion of // nidcradcnia was \](i[ accompanied by 

in Holocarpha revealed that intert)opulational crosses development of inlersltMllity ^\ith (dosely-related 

within each of two widespread, taxonomic s|)ecie>. // 

embers of IL rirgata; conversel 



on n 


heermannii (Greene) D. D. Keck antl //. }irgata (A. 
Grav) D. D. Keck, were either unsuccessful or \ icltlcd 
inviable or sterile hybrids (Fig. 12: Clausen. 1951). 
Chromosomal studies revealed karyoty[)ic differences 
betAveen iutersterile, often morphologically indistin- 
guishable plants from flifferent populations (Fig. 15: relatively rapid rise of//, macradcnia. 

intcrsterilit) between "conspecific'' lineages within 
//. nrgala (and //. heermannii) was accom[)anied by 
relati\elv minor or insubstantial phenotypic di\er- 
gence, despite longer evolutionary tinu^frames for 
>ucli divergence to have occurred compared lo die 

Clausen, 1951). Clausen (1951: 99) concluded that 

Based on available data, Ilolocarpha macradcnia 

chromosome evolution via structural rearrangements appears to represent yel an(ttlu;r exami)lc among 
had resulted m eacli population of//, heermannii and continental lanveeds of a perii)heral isolate that 
H. virgaia becoming "a breeding unit by itself and 

luiderwcnl rapid morphological atid ecoiogi 

loirical di- 


Annals of the 

Missouri Botanical Garden 



« * 1 


an Dieqo 


Byron Rd. 

O Minkfer 


F| almost fully fertile 

F, partidlly sterile 

F| completely sterile 

F| as embryo only; no qermination 

Crossinq failed 

mmm Limits of species 

l^'i^lHL" 12. 

populations Iti //. hrrrmtninii and //. rirg,il<i, lii-]i nilerlf ililil\ amtMi^ popnlatiijns of //. ohronini. and partial Icrtilits of 
li>lnids hrhvrcn //. /namidenia and //. nrg<ifii. licprintrtl from S!<i^rs in llic Eioiniion i,f riun! Species. ])\ jrns Clausen. 
C(>p\ri<^lil ® 19r>l liv Coiiifll Uni\(M-sity. I'scd l)y fxTniissinn (tf tlu- jitildisliri'. (]orn(dl Univ. l"*ivss. 

xrrgencc in a \u)\c\ luihital. Vtilikr oilier in('ml)ei-.s oC Coast Ivaniics 

u « 



])r(i\ Hlf'd tfio (lr\ intorior liahilats 

I/olocarpha, wliicdi aro found extei]si\(-dy in interior nr now so ooniplolol)' o\[)loilc(l hy the [liree i]ilerit)r 
southern Califortnan habitats with e\tretn(dy clr) , hot s])eeies" (Chiusen. 1951: 107^). Pahiier {\9iV2. 1987) 

sununer climates. //. inacradenia oe( ur; 

s on CO 

terraces in llie San bVancisco r>a\ atid Monterey Hay 

areas, Avhere sutniner di'oughl and hMiiperalui-cs are 
»ireatly anudiorated l)y on.shon^ winds and lo^,. Clausen 

siiii;<^'esled instead thai //. 


/fi(t(Tft(l('ni(j atose 



inenihers ol //. virgala thai iti\aded ihe e(»aslal 
during an uiiusualiv warm 


ptM'iod wilhiti the last 
10. 000 years. He based his h_\podiesls in pari on 
(19.)1; lOS) suggested that //. mdcmdcnia and H. patients oC chromosome e\oluti(tn and interfertilitv 

widtin afid IxMween llie t\\o laxa and on moiphologieal 
eoiisid(aalioirs, iiududin^i^ a suggestion I)) Carhpiist 

iiiLdsla ''...probably were intercoimeeled as maritime 


1 inl: 

races o( on(^ species before the Coast 

I^uinges arose/' lie fLntlnu- positetl thai tlu^ ilse of the 

(I9~)9a: .'505) tlial dislin(diye dislaldeaf morpliolog)' of 

Volume 93, Number 1 


Clausen, Keck, and Hiesey Revisited 


Fli^mc l.*^. lllustiatlons of.ioinatie chruinosotiH- sets from loot-lip [)i'('| )aiali()iis for r('])r(^sciitati\ cs i>[ difffi-cnl i)o]uilali(nis 
ati<! s[i<'cics u{ llDliHtupha (diit" cliroiiiosonip of each pair is shown). \nW exirnsivr chromosomal varialion among popiihilions 
of//. Ijecnnannii and //. lirgata. Rcpiintcd from Stages in ihc F.i'oli/fion nf PIdu! Species. h\ Jens Clausen. Copyrin;hi © 197)1 h\ 

Conifdl rni\ersil\-. Tsed l)\ permission of thi^ jiuMisher. Cornrll Vw'w. I'i-ess. 

il. nuicradcnia may represent merely "a juvenile previous seeliou). In eonlrast. tlie puleutial cNoliilion- 

f the (llslal-lt^af eoudilitiu iu olliei" taxa of ary imp(irlaiu:e of ecologieal seleelion in tlie di- 


orm o 

vergeuee ol liypolliesizefl peripheral isolates in holli 

Holocarphd. Molc^eidar pliylogenetie data are most 

cousistiait with Palmer's (1987) evolutiouary scenario; L(iyi(i und Ilolocarpha is difficult to ignotx- (dimatic 

the actual time of divergence of//, mdcvadenia is still 
under investiiralion. 

and/or edaphie differences between hahilals ul 
paraphylelic "[)rogenitor" taxa and nested '^leriva- 


As in the origin of Layid discoidea, evolutionary tive"' lin(^ages are extreme. In Ilolocarpha, ecologieal 

{'Ilolocarpha nuicradcnia was not accom- selection also may have played a significant lole In 

an'enrencc o 

maintaining long-term phenotypic stability among 

panied hy ae(|uisilion of strong internal ])arrlers to 

illi close relatives: Clausen, Keck, and morphologicall) cr)[)tic, intersterile lineages uitliin 
Hiesey produced a vigorous, partially fertile F2 //• hccrnianuii and //. rirgata; genetic cohesion hy 

gene now w 

gene flow cannot explain morphological .-lasis m cacdi 
of lh(^ two laxa. 

generation front crosses jietween //. macradenia and 
H. rirgata ((Hansen, 19.S1). Given the great potential 
foi' (duomosomc evolution in Holocarpha, Uie lack of 

tTiajor (diromosomal repalterning associated with AuAPriM-: liADIATION AXDTIIE "Madh PArrrilX 
e\-o]utii)n of the distinctive //. fnacradenia is consis- 
tent with di(^ conclusion from studies ol L. discoidea 
that genomic r(M)rgani/,ation may be less important in 


rapid evolutionar; 

\ (Uve 





Clausen, Keck, and Hiesey's biosystematic Inves- 
tigations in Madilnae led to recognition of extensive 
rgence of peripherally isolated hitcrsteriHly l)c[ween species then treated as nuaiilx'rs 

u{ Madia Molina (Fig. 17). Clausen (1951: L'Vl) staled: 

las been widely suggested (see 


Annals of the 

Missouri Botanical Garden 


M^ur(\-. I I and !o. Kroloyicallv s<'[)aratr(L parlialh iiitiTfcrt iU- iiicmiIxts (tf /7o/(KY//7>//f/ wild (our pairs r)!" {ln-oniostHncs. 
Fi^tjrr 14 (left). Ifolocarplui rir^vta. — A. CapilulcsrciUT. — H. iii\(.]iu lal in-.wl (al)a\ial \\c\\). — C. Disk Ilnrcl. — D. liav 
fruit (adaxial vii-u). Figure lo (ri^i^hlj. Ilolorarphfs mucnuU-n'ui. — A. Ilahil. — H. Suiii segiucnts. — C. Capilulrbrrntr. 
— n. fiivoliicral ])ra<-t (ahaxial view). — K. Disk CKuvl. — F. Hay Iriiil (a(ki\ial \ie\\). — C. Ra\ fi'iiil (lateral \iru). 

'The species ol Mftdia are evloloiiieallv and <ieneli- 
{■ally much tnore is()lal(Ml from eaeli oilier lliaii ate llie 
Tax ias. . . .Mu.^1 u[ die species o( M(uli(i can he linked 

sensu (daiisen (D).'SI; Fig. lo) also included planls 

)ee[i j)laced in \\m' utams: two 


never ha( 


from tiKaitane ('aliloinia 



I(.gellier [lnoii<j;h h\l.rids, hut llirse are sterile, and, scahridns (Kaslu.) I!. C. Balduin [= llnillardiopsh 

tn(jre(»ver, many hyhrids have unpaired, nonliomolo- scabrida (i^astw.) Ryilh.J (Fi^i^. D)j and Ciuiqiiislia 

gons chromosomes. ^Fliere is, ihereforc, usuall) only muiiii (A. Crax) H. G. Haldwiii [= Raillardiopsis 

one species lo a species complex in Miulinr In iiuiirii [\, i)rd\) livdh.J (Fig. 20) — atid the endetnic 

(lesii!^nating fi 

^ gcnm-al eat(^gones ol ierlilil} j)atlerns 


Hawaiian sllversword allianc(^ a nu>nopli\ icLic gioup 
iti \aseular planls, CranI (1971: lOJ) aplly t'oiisideriHl coiu])rising .'}() woody ajid semi-woody sjieeies in 
^■ihi' Madid pallenr' exemplar) of "afnitial herbs Argyroxiphliim \)i:,J)iihauli(i (]i\m\n-\\.. and WUkcsia 
wilh. ..relaled species usually separated l>y incom- A. Cnw (Bahhsiti et ah, 1991: Daldulii. 1992. 199(k 

pallhllitv harricu's and hv ehroniosomal ati( 


2(l():5a; Harrier et ah, 1999). dlie two Callfonnan 

stei-iJily harriers." As ree(.gni/ed h) Clausen (I95I) peremihds {A. scdhrldus and C. niuirii) atid the 
and Cranl (1971), sterilitN I)arriers in l/r/r//V/ and odier silversword alliance were not shown coiR]ncin";K to 
plant groups exhihiling llu^ ''Mudia paltern'^ do nol he niemhcrs of Madiinae until puhlicalioii of Carl- 
necessarily pj-celude r.'tieulale evolution; Clausen. (piist's (I9S91)) anan)Miical invesligaliotts. afler Clan- 
Keek, and lliesey (1917)) demons! taled that \ igorous, stau Keek, and liicse) concluded their experimeutal 
hu-gely sterile hyhrids in Madia had considerable studies of llie suhlilhe. Carlquist (19r)7x 1974. 19()(l) 
l»"l''"'li:>l f*» produce fertile, stable, allo[)oly|>loi(| also eham])ioMed ihe h)polh(-sis that the Hawaiian 

taxa re^preseiit a major example of insular a(la|)li\* 
radiation. The silvetsword allii 

nice nicUK 

les t 


lineages, such as their synthetic "M. iiutranimii" and 
the wild species, M. cilrigracilis 1). F). Ket:k. 

Suhse(juefi[ niohM-ulai- phylogenelic studies of shrubs, mal-platils. cushion plants, woodv vines, and 
Ma(hiiiae and relatives revealed thai Madia, as rosette |>hnits. spans most of die \vid<' speetrinii of 
Uealed in all pre\ lous senses, was not mono|)hyletic; habitats (outid in ihe Hawaiian Islands fiom <lr\ scrub 

the smallest clade encompassitig all spceies ol' Madia 


100 mm rainfall/yr) to rainforests atul bogs 

Volume 93, Number 1 


Clausen, Keck, and Hiesey Revisited 







0.001 substitutions/site 

Pi if lire 

16. I'll) logdu'tic hypotliosis ((inc n( Iwo maxi- 
riialK parsimonious liees) fof Holovarpha nuunidciud and //. 
rira-dhi based on analvsis of nuclear loS-26S rl).\A (^vlernal 


and inlfinal Iranserlhed spaeer (ETS and Id^S) secjucnees 
from representatives of 1.'^ widfdy-separaled populations 

(Baldwin, unpuhlished): t[]r elade sliown is from a larger tree 
ineluding represeiilalives of //. heermaiinu and //. <)h<-(Ht{.c(t 
and oiil^nnip Laxa in Dcinandni [D. conjugcns (1). I). Keek) 
B. C. Baldwin and D, JusncaUitd (DC.) (w-e*Mie]. Hraneh 
lengtlis eorrespond lo relati\e lime sinee diveigenee. under' 
maxiinuni-likeliliood oplimizalion; rale eonslaiicy of ITS 

not Ije rt^jeeled u>iug 

e\ () 



across lineaues could 

Felsciistein\s (1988) likelihood-ratio lest. Numhrrs aloiip: 
brandies are parsimony bootstrap values (only \ alues > 85% 



groiij) iiiito themselves'' (Keck, J 936: 10), although his 
iiudusion of Wilkcsia in Argyro.xiphJum has iiol been 
uidudd (Carl(iLiisl, 1957; Carr & Kyhos, 1986; 
Bahbsin et al., 1990: Bal(K\in c^ Robichaux, 1993; 
Baldwin. 1997). At the same lime, Keck rcjccled 
Gfay's (1852) placement of Argyroxiphiuiu and 
Wilkesia In Madiiiiae and sLuinised thai the silver- 

ilhoul close 

relatives" (Keek, 1936: 10). Keck (1936: I I) 


alliance was ". . . j)r()l)ably w 

eon(diHl(Ml: "By thus (h\(ircing Argyroxiphiuiu Iiuiii 
ihe American genera lo \vhi(di il has ])eeit thought 
related, the most persisleiitly proposed conncclion 
between thi' ancient element in the Hawaiian flora 
and llie New World has Been shattered." 

M(dcciilai- phylogenetie data on historical ec<dogy 
and on liming and rate of diversification of the 
Hawaiian silversword alliance upliuld Carl(|in>t s 
(1965) hxpotliesis that ihe Hawaiian taxa repres(Mit 
recent ada])live rachaliuu from a tanveed ancestor 
T^illier than an ancient lineage wilhonl (dose rtdalives, 
as suggested by Keek (1936). Bas(Ml on rI)NA ITS 
trees, OsbortTs (1902) original, ecological criUM'ion for 
adaptive radiation is met by the silversword alliance; 
major ecological shifts between wet and dry habitats 
were evident!) associated with diversification on ea(di 
of the hiur majoi- island grou|>b occupied by the 
h'ueage, with the possible exception of ihe youngest 
island Hawairi (Fig. 25; Bahlwin & Robichaux, 1995; 
see also Robichaux el ah, 1990). Simpson's (1944) 
rapid-(hversification criterion for adai)tive radialion 
is also mel; inability lo reject rale constancy of 
molecuKu- evolution across clades in the ITS Ihm's and 
time-cab btalion of a nod(^ outside the Hawaiian 
lineage allowed estimation of a maximum age for the 
most recent common anct^slor of the silviM'sword 
albance at 5.2 ± 0.8 millitm years and a minimum 
diversification rate for ihe group of 0.56 ± 0. 1 7 
species per million yt^ars (Fig. 26; BahJwin c^ 
Sanderso!!, 199o). The estimated maximum age of 
the siKcrsword alliance is roughly comparable lo the 
age of the oldest modern high-island, Kaua'i (ea. 
5.1 million years; Clague & Dalrymple, 1987) and 

(> 12,300 mm/yr), and extends along an cIe\alional mucdi younger tlian the > 10 million-year-old esli- 

gracnent from near sea level (75 m) lo high ali>ine 


mated ages of some other [)rominent examples of 

(3750 m) (Figs. 21-2 1: Carr, 198b; Carr (^l ah, 1989; adaptive radiation in the Hawaiian Islands, such as 
Robi(haux et ah, 1990; IJaldwin & Roi)i(diau\. 1995; Hawaiian drosophilids (Thomas & Hunt, 1991) and 

Baldwin, 1997, 2003a, b, c). 

lawaiian lobelioids (Givnish et ah, 1996). The 

Clausen, Keck, and Hiesey w^ere aware of Gray's minimum diversification rale estimated (or the sdver- 

(1852) early itK hision of the Hawaiian gciuaa 
An(yroxi})hiuni and Wilkesia m Madiinae; Keck 

sw^ord ailiant-e falls within ll 

le upper range of 

estimated raters for various continental radialions of 
(1936: 8) conducted a systematic study of Argyrox- plants and animals and was regarded l)y Nee (2001: 
iphiuni "...with the (,'xi)ectation of treating II in ... 661) as "remarkably high." 
Ma(h(i)nae," and aslulely suggested thai members of 

An expanded perspecthc on Madia that encom- 
the Hawaiian silversword alliance, as currently passes all of the "Madia" lineage (Baldwin. 1996; 
recogni/ed, ''...wotdd appear to constitute an insular Fig. 18), i.e., the elade intduding all of the taxa in 


Annals of the 

Missouri Botanicai Garden 





• « 





P ' 

*-^ ^P.M 

I ^ 

%.■■'', ■'■ ■■ —: •■:•■ 

Species Complex 
Fully fertile hybrid 
Partially sterile ' 
5tenle hybnd 
Crossinq failed 



Figure 17. Cros.siiit; (Jia^mni u{ Xhidin .sciisu CkuKsrn (I'All). i-Lill\ iiilci-ft rlilc la\ii slinwn in llic dia^rarii aiv iinu iroalcd 

as ln\(HH)[tiirally indislincl [Madid capitahi Null, aiul M chili'nsis (Nutt.) lii'ichc aiv now tivalcd as sMioiiMUr. of U. sadni 
Molina, Miidta uheeleri (A. (wav) f). D. Keck is unw trealcd as a s\utniMii nf ][. clcgans I). Dnti ex I.JiidL). Souic spt-cics arc 
ui>\\ livahil in odicr ^taicra. i.e.. \n!sncfiri)iis \ull. | 1. nuidioidi's \y\[\.\. Ihtrmouin W. i]. Baldwin | //. huUii (I). I). Keck) \\. (\, 
Biild\siu, //. antdus (Grriau-) U. (;. lialduiril. Ilrnuzi^nclld {\. {]n\\) \. Cra\ |//. iniainui (A. Cray) A. (iravj. ./r/^.s/V/ W. {], 
Haldwin |./. ra//?m// {(Wccuv) W. (]. Bal.lwin. ,/. yi>scinU(in(i (Parry ex A. Gra)) I], C, l^alduuil. and Kylwsia V>. C. liahluiu [A'. 
holandcn ( \. (way) H. (i. I^a!d\\iu|. All la\a shown are aruiuals e\eep[ \in- .\nisnr<trpn:^ madioides and Kyluisia Ixdaadvvi., whic-Ii 
;uv |)ereninal lierhs. The ''Madia" linea<ie (lialdwui. 199(>) alsc inrlii<les Anisocarpjis sciilniilus. (^.nrlquislid luuirii, aufl (he 
Hawaiian silver^word alliatiee (^JO species in \rii\ nniphiiiin. Didmului. and II ilkcsid], R<'printed Innn Stages in llic fJiolnfian 
of Plani Species, hy Jens ClauscMi. C.>p\ right ® \^)r>\ in Cornell Uui\er>il\. Csed by pennissinu of die ])ul)li>licr. Cornell 
Uin'\"crsil\ l*i"ess. 

lal Ic 

ii'\\ee(ls iti general) are (h\arfc(l !>)■ adaptive 

Madid scnsit Clausen, Keck, and iliescx (k'ig. 17) pins ncii 

Aiiisocdrpas srahridiis, Carhjiiistia miiirii, and die i-adiation oi' [hv Hawaiiian sih crsuunl alliance; llie 

Hawaiian ^iKer.sword alliance, reveals sln>n<,dy con- continental laxa of llie groii]) arc aniinal and |)crcniiial 

Irasling pallcrns of plicnolypic divergence. Life-form heii.)s dial occnr along a rtdallvely narrow prccipila- 

evolulion antl hahilal sliills among conlineiilal lion gi'adlcnl comparfMJ lo die wide I'ange of diy, vvel, 

memhers of the "Madia'' lineage (and among conti- and hogg) situations occn[)icd h) die semi-woodv and 

Volume 93, Number 1 


Clausen, Keck, and Hiesey Revisited 


Arnica mollis 

Hulsea algida 

Adenothamnus validus 

<70% bootstrap 
>70-90% bootstrap 
>90% bootstrap 


Hemizonia congesta 
Blepharizonia laxa 

"Hemizonia" lineage 



Carlquistia muirii 

Madia elegans 
Jensia rammii 

Jensia yosemitana 


Argyroxiphlum sandwicense 
Wilkesia gymnoxiphlum 

Dubautia laevigata 



Anisocarpus scabhdus 

Anisocarpus madioides 

Harmonia stebbinsii 



Harmonia hallii 

Kytiosia bolanderi 

l-lemizonella minima 

Holozonia filipes 

Layia chrysantliemoides 

Layia lieterotrictia 

Lagophylla minor 



Achyrachaena mollis 

Blepharipappus scaber 


Centromadia perennis 

Deinandra greeneana 

Holocarpha virgata 

Osmadenia tenella 

Calycadenia fremontii 


50 changes 

Figure Ml. Pliyloirriirtic In pollicsis (llic most pjirsinionioiis tree) for Madiiiiae based on siiiiu]laiHM)us ana])riis of 
chloroplast DNA (irnK Iiili-on) iiiid 1 MS-26S iiiiclenr ril^osomal DNA external and internal Iranscrihed spaeer (ETS and ITS) 
sequenees (Baldwin. 'lOO'An. impuhli^lied). The dark l»ox ne.sled wltliin the ^"Madia'' lineage eneloses the elade eorresponding 
t(t the Ihuvaiiaii silversword aMianee (Argyroxiphiiini, Dnhaufia, and Wilkcsid). Ast(^risks (*) indieale ihat hraneh siipporl rises 
to the next h-vel indieat(nl by hraneh widths wiUi rtMHoval of sequ(Miees for the three lung-hraneh, inonolypie genera: 
Achyrachdcmi Sehaiier, BIcpharijKipptis lhK)k.. and llulozoida Cnrene. Raillardella (A. Gray) BenUi. is represented l)y a tvuY. 
intron seqn(Miee of A', ari^rnlca (A. Cray) A. Cray and m'S and ITS sequenees oi R. pringlei. AUopolyi)loidy of the TIauaiian 

(I]arri(M-<^t ab, IWOJ is not resolved by ehloroplasl DNA or nnelearrDNA sequ(uiees. See Appendix 1 for 



1 Ulllc 


authorship of s])eeies names not mentioned in lexl. 


Annals of the 

Missouri Botanical Garden 















[/ ■ 



'■ i 



, 1 




h<^iir('s 19 and 20. Califomian nioMtaiic pcrdiiiials of llic "Madia" linra<j;(\ iinl iiirliulfnl in Mailia scnsu Clausen 
(195J); allliDii^li l>ulli diploid s|H'ri(\s wcrr |> Ircaird in luiillardiopsis R\(ll).. llic grnonn- of racli is cvidiMitK niorr 
closfly rrlatrd lo a dilTcrrnt ^riionic In [\u- (alloUlr-aploid) Hawaiian siKcr.snnid alliance lliaii to llir geaionic in dir odiir 
diploid (liarnrr r[ al.. 19Wj. Kigino 19 (l.-fl). \nisnc(irjni.s scahridus. —A. llahiL — B. Leaf. — C. Ilrml. — D. \la\ lloivf. 
— E. Disk [Intel. — F. l\a\ Iruit anti liall-cnvcloping involucral hract (()lili(|ur]\ ada\ial vicnv). Figure 2(J (riglil). G//7(////.s7m 
niuirii. — A. Ilahil. — H. l.eai. — V.. Head. — I). Morel. —V.. Frnil widi paj^piis. Bodi species have Ixmmi iiuolved in sueccssrnl 
crosses with ene anodier and widi nieinhers i)\ die Hawaiian silversword alliance (Baldwin et al.. 1991; Carr et al., 1 99(); 

Ba!Ti(M- et al., 1999). 

riiyl()g(Mi(Mic evidence- (or oriiiln of the silversword 


woody liauiiliiin species (sec Haldwin, 20():^;i. Ii. c). hclween the {•onliiicnlal perennials and hetwtM'n the 

c(tnliiiental and Hawaiian perennials of the ''Madia'' 
alliance alter (■onsi(hM-al)le (h\'ersi(icalioii of ihe lineage, not afteniplcd hv Clansen. Ketd^, and lliesey 
'"Madia" litieage (Figs. \\\, 26; see also l>arri.'r et (see Fig. 1 7), either ha\e failed or yielded \ igorotis F, 
al., 1999) intheales that ecological dl\crsit) in tlie hvhrids of exlivinely low pollen stainahililv (an 
Hawaiian lineage represents a major accc]crali(»n of estimate of ferhlit\), with most -tainahle ";raiirs heiin 



evoKitl<Miary (diange assoeiat(Ml with coloni/ation of ahnormally large, lelraporate, and pntali\el) dl[)loid 

(Kyhos cl ah, 1990; liahlwin et al. 1991; Carr et ah, 

ihe Hawaiian Islands, 
oceanic-island lineaaes ii 

As snggestf'd (or diverse 

i^v I general, a(lapti\-(^ radiation 


1996; Harrier et al.. 1999). ()|.ser\ed lack (»f 

f the slKcrsword alliance pnjhahl) lias Been in inlcrhnillity Between the conlinenlal penaiinals and 
large ])art a eonsecjuerice of ecological opportnnity B<'l\\e(Mi the conlinental and IBnvailan perennials 

Sini])son, 19.1'}; see Sclduler, 2()()()), ultli a\alla- conforms lo the resnlls obtained l)\ Clansen, Ke<l, 
bilily of a wide array of empty nhdies in th(^ and lliesey foi" the atunial nKMidxa's of the lineage 
Hawaiian islands and lack of inlerfenMice with ((danseii, 1951) and lo the ''Madia paltern" descrli.ed 

olher organisms, j)ossil)ly aided 1)\ intrinsic factoi's By Grant (1971). In contrast, crosses Belwcen 
promoting e\-oIntionary ehang(\ such as the 


memBers ol ihc Hawaiian slBersworrl alliance lu 

i\ e 

polyploid constllnliun of the group (HarruM" el al.. yielded \ igonnrs. partlallv to fnllv hM'lUe hvBrids In all 


interspecific- and lnt(M'generic coml)inali(ms al- 

Kxtension of (dairsen's (1951) crossing icsulls to lenijited, despite majoi- moiphological and ecological 
encom|)ass |)erennial memBei-s of the ''Madia'' lineage divergence of the ta\a (Fig. 27: ('arr tK K\hos, 19i5l, 
has indicated strikingly dilTcnmt fertllit) patterns ]9{]6; Carr, 1985. 2003a). Reduced fcrtilil^ In some 

belweeji the continental and Hawaiian taxa. Crosst^s 

Hawaiian hvBrul comBi nations can Be altilBnIed 

Volume 93, Number 1 


Clausen, Keck, and Hiesey Revisited 


Fi-Lircs 21-24. MtMiihors of llie Hawaiian silv(M-s\vf)r(l alliaiKc Kigtitv 2] {upper left). Ar^^yroxlphiuni sandwlcense DC. 
siil)si>. marnx-ephahuu (A. Cray) Meyrat, a iiioiiocaipir. lliick-leavcd rosellc planl of dry, al|)inr, cliulci- slopes and Hats on 
llalrakala. Kasi Maui. ^A. Habit. — B. Head. Fii^mv 22 (up[)<'r H-lit). Duhaulin ladjolia (A. (iray) I). I). Ke<-k, a liana (woody 
cliinber) of tn<!sic lo url forests on Kaua'i. Fi-ure 2:5 (lower lefl). Diihaitlia reHruUiia (Sherff) I). I), keek, a tree or large shrub 
of wel forests on EasI Maui. Figure 24 (Iow(m- right). Wilkrsia <(ymno.\iphiiim A. Gra\. a inonocarpie, fibions-leaxed rosette 
plant offh-v slo[)es and ridges on Kaua'i. —\. Ihibil. —P.. Seginetil of eapitulescence. ^C. Head and distal peduiiele. 

tnoslh or solely Id one lo three whole-arm reciprocal 

shown to serve as effective pollen parents in back- 

translocalions that tbfferentiate genomes of the groiij) crosses, uith recovery of full fertilit} iii a Mibset of B2 
(Carr & K) hos, 1986; Carr, 20031)). Even hybrids of i)rogeny (Carr, 1995. 2003a). Ecological f]iosl-dis- 
low fertililv. i.e.. \n'{\\cvn Argyroxiphium sdiKliciccnse 

[)ersal) selection against hybriris ap|>cars 

to he 

DC. suhsp. macrnccphdhim (A. Gray) Meyrat and Important in limiting gene flow in ihe Hawaiian group 

(Carr, 1995), although snth selection has not pre- 

Duhantia nicnziesii (A. Gray) D. D. KecK, nave i>cen 




Annals of the 

Missouri Botanical Garden 



* Y 



Kaua'i or 
Maui Nui 





'^ H;n\ai'i 

50 km 









m -^_^ 









■ fc- 

^ ^^^ 














































m ^_^^^ 











H, RP, orS 

RP Maui Nui 
or Hawai'i 

CA FP, Kaua'i, or Maui Nui 















our' iM'iiii 



Figure 2.^ (pit. Hl-87). Ecolu^uical shills ;iih! itiMJor tli^pci^al r\rnl> (iiiriM<i (livrrsificnliini of each of 
lineages (if llie Hawaiian sil\ rrsword alliaiicr, hased on ifie senil-slrlii r(ai>eiisu> of ci^ulil inaxlrnali) parsInKniidu.^ mieleai- 
iDXA ITS lives (ivprinted or adajiletj (nini H.dduiii. 1*)<)7: dala fioni Bal<luiii ^K rn.))ieliaii\. 1995). — A. AritMD.xiphiiun. 
a \eLaig-i>laiid nronp (Maui and lia\sai-i). slioun in eoiitrxt i>\' "Duhdufla/WilLrsKi" Wnnvj^c (detailed in Mgs. 2MI C. and D) 
and ueslern Xojlli Aineriean tml-toup la\a — ninnlanr. pcreninal larueed> (»( llie "Madia'' linea,iie (in Anisocarpiis^ Cdrhpiisf'uK 
[\\\i\ kyht)si(t). — [}. WUkcsia and sister grouji (pail iA' Diilxiuliu), fesltlctcd lo Kaua'i. llaMlal aMaevialiuns and ^\ B = 
hog; D or sun s\rnhol = dry: W = wet: cloud synihol =^ wel or h.)g. Ihihit s)inhol^: II = herh; L = liana (wot^dy e]Iinh(aj; .\1 = 
mal-planl: RP = losette ]flant (nion(M:u-pie or pol\ earpie); .S = shruh: T ^ live, (ieograiiliic ke\: CA KP = (^aii(oi-nia Kloiislie 
I'rovniee; Mam \ul = prehistoric i>hui<l uuiling Lana'i. Moloka'i. and Maui (and Kalio^thnve. whore no rneinher> of Madiinae 
are known lo occur). Placement oT geographic area. hal)ilal. and hahit along hianches is \\hrr(^ ancestral stale i.s une(iiii\()cal 
hased on j)arsinion_\ criterion (Hahh\in cK Ktihichaux, I99o). Island occurrences an 
aMiance conlmin with Carr (1'>(5.'S, 1999). Taxononiic ahhroviations: 1. saiidn-icciL^c- 
suhsp. sajhJu'iccnsf: I), ciliolala (!>('.) I). I). Keck 

lilt'~[oiiii iiilorination for the siI\'ei's\vor( 
- "///." = subsp, HKicn/ci-plitilimi. ^\s." = 

— "c." = suhsp. cilinhfffK "^'-.^ = sn!>sp. niiiiinosa C. I). (Jarr; I). Liiitdsejiii 
•;/■" "^ ^u\)>\).J"difi)nnis C. I). Carr. ''kr ^ huhsp. hiudsrnii. "//." = suhs[). iKii^raiar flL Si. John) (,. I). Carr; I). I<ix<i 

Nook. lS.' Arn.— ''hr = suhsp. hirsida (]liilcJ>r;) C. 1). Carr. ^7." = suh.sp. hrxn: I). Unraris fCaudlch.) H. 1). Keck— "//.'' = 
suhsp. Inllchrandii {II. Mann) C. D. Carr. -/." = snhsp. linraris: D. pJ<in!<igiiH'<i Gaudich. - "BlI" CTduo 11. )h-"*) = sul»>p. 
inag/iifniiti (Sfuair.j C. 1). Carr. "h" = suhsp. Ituinilis C. I). Carr. •7;."" = suhsp. />/a///(/-//;c./: f). snihni (DC.) \). I). Keck— 
■7." = suhsp. l('ii)ph}U(i (A. (iia)) (;. D. Can', "s^ = .^uhsp. srahni. ^rv \ppen(h\ 1 for authorship of s 
iTuaitiorK^d in to\t. 

jiecies names no| 

(dinled (^staMi:>hnic'nt of liyhi-ids; :?o nalui-alK oceur- 

e.g.. fof I), scabra (DC.) I). D. Keck (Uahlwin rt al.. 

liyl)|-i(l coinjiinalions Itelween diffei-ent ])airs of 1990: IJaldwiiu 1997). 

species (ifudndiiig intcrg(Mi(M-ic h\bncls) lia\c hccn 
docLiinculcd 1>} Cair (200;5a). and e\ ideiice fur both 

I : 

Ilic stark ctjiilrasl Kctwecn tlie Hawaiian pallern of 
iiiteilcrlilil) across pli(aH)ly[)i{-ally dispafalc liiieagi^s 
ami \\\c paltcrii ol inlerslcrilily seen acioss the less 
dislincli\(' continenlal species of the "Madia" lineage 

recent and ancient introgression has IxM'n obtained 

from slu^llcs of hybrid /ones (Grins el al.. V)a<\\ 

Caraway (M al., 2001) and comparison of ph\ logcnetic ha.s e\ olulionary impllcallons. Lack of strong, intrinsic 

data from cxlogenetic, niudear rU^A. and chloropLisL repro(hict 1\ c barriers belween specl(^s and genera of 

DNA studies (nalduin et al., 1990: Baldwin. 1997, 


the Hawaiian siKersuord alliance ]ea\es open tl 
2003c). Hybrid specialion, as well, may explain some pcjieiilial lor lnunoph)id hybrid sj^eciatlun or iulro- 
condicLs be(v\een dillerent lines of pInlo<'en(Hic tlata, 

1 4^ (_ / 

gressn)ii involving plants 



(hllcr iireatb' 

Volume 93, Number 1 


Clausen, Keck, and Hiesey Revisited 




Fi^uif 2."^. 



















Kaua'i D or W 

















orni or 

e n V 1 1( ) n m e 

tlial successfully co 

(lialdwin & Sanderson, 199i5) allows patU^rns of 
iiiltM-ferliliLy to be placed iu an uuderslaudabU: 
perspecLive (Fig. 26). Lack of inlerfertility belween 
continental perennials and hctueeu continental and 
Hawaiian perennials may he explained simply by the 
loiiger linieframe for evolutionary div(n-gence Jjclween 
those lineages compared to the time since divergence 
of the Hawaiian lineages from a common ancestor, 
willi gradual breakdown in inleif(Mlility through lime 
as a by-product of divergence. Interfertility between 
members of the silversword albance is consistent willi 
ferlilily patterns seen in other (mostly perennial) 
lineag(^s of Hawaiian angiospernis ( Carr, 1998; 
Ionized the Hawaiian Islands Baldwin, 1998) and conforms more closely to the 

ecological setting, particubuly under 
nlal conditions ravora1)le to recomlnnant 
plieiu.lvpes (Carr, 1995, 2(H);^a). Intersterility barriers 
among continental species of the "Madia" lineage may 
limit ihe evolutionary potential of hybridization to 
formation of allopolyploids, as demonstrated experi- 
mentally 1)y Clausen el al. (19bS) for some annual 
sjxjcies and as meiotic belunior and diploid pollen 
formation indicate for hybrids between the continental 
peremiials (Carr et al., 1996; Harrier et al., 1999). 
Such allopolyploidy has contributed only modestly to 
di\ersity in the continental lineages (e.g., Madia 
cilrigrarilis), but evidently gave ri>e to tlie lineage 

and became the silversword alliance (Hai-rier et al., 

1 999) . 

eonimon fertility pattern seen in voung woody plant 
grou|)s in general, i.e., the "Ceanothus pattern'' 

rhyh.genetie data from IfS srHpi.-nces on time (Cant, 1971), than to the -Madia pattern," seen 
since^l.vergenee of pere.mlals in the "Madia" lineage widely in annuals (Grant, 1971). Although the relative 


Annals of the 

Missouri Botanical Garden 



v^^ -i ,.Ck 















■ U 


















Kaua'i W 




T — 



















iiic -:o. 


(.. M(Miil}ft's i]{ Dubdiiiid with u<'iu 


pcrs. c'oiiHii.)- nalivr (l>ii[ nf>l nil iMidctnic) lo KaiKil. — 1). Duhaiifid scd 
(uol on KiiiiM^I). For nildiliofinl ([claKs. scr p. 84. 

ai-raii^urnu'iiN DCA and YnVA (Cair ^X l\\li<)s. ITO6. 

RailiKiid'm^ rcstiirlcd to one or inoi-o \oinm islaiirlfs) 

liming of (li\('r*i,('iu'e (;f aniuuil> and pereimiaU in die CoMJ.l -in\s 

"iMadia lineage" has not yt;! been resolved, the 

generally higher rates of id).\,\ e\olulion in die 

annuals eoninared to die perennials (Baldwin S; 

Sanderson, 1998) aecords widi findings (or some 

Kvohilionaty in\esligalions of ATadiinae in llu^ wake 
oJ (^lansen. Keck, and iliesey's pioneering researrh 
liave led to a greatly expanded eireimiserlj)lion of the 

: of 

otiier angiosperni> (e.g.. Sidalccu \. Cra\; Andreasen MJ)tiihe and a nion' detailed underslandin 

t'v Baldwin. 20(11) and iTiay reflect more general rales i)roresscs and patt(M-ns of di\ ersificalion In ihe gronj). 

o( mol(M'ular evolution, which, in Inrn, cotdd hear 

a pulalively higher rate of actpiisition of post-/ygotlc Mailiinae throngli 

reproducllve l>arri(M-s hetweiMi atnuials tlian hetween 

I)erennials in gcnerah Sinnhn- results ha\e he 

Proirress in resoK ina evolnlionaiy ([nesiions in 


^.. nitegralion of diverse^ I i ties of 


evi(l(aic(^ follows in the tradition of Clausen. Keek, 
and lliesey and n^affii'ms the valui^ of s\'st(Mnatic data 
ohtanicd ni com])arisons Between phylogeiielic and foi' tackling [>n)cess-oricnIed evolulio]iar\ (juestions. 

data lor continental annual and insular as appreciated h\ tln^ Cai-ne£rie learn. Clausen. Keck 

cross] ng 

t)erennial lineages of the larweed genus Dcinaiidt 
Greene (Baldwin, unpuhlished). d^K^sc findi 


nniuirs re- 

geuelic (diange and 

and lliesey's e\i(lence h)r a d\naniic e\ ohillonary 


history of Madiiuae, holli in relalive rates of 
inforce Ci-anTs (1971) ol)S(a\atIons on associations moipliologlcal. ecologicah and 

among life hislorv. patterns of iiiterfertilily, and die in mod(^s of di\ er.Mficallon. has l)eeu u])h.dd and 
evolutionarx polenlial of hv hridi/atinn in plants, and ext(aidc.l to finer-scale lc^eI^ ihau in the comparisons 
dlustrate nudicrcontra.-^t.. in patlerus and procf^ssesof atnoug genera descrlhed B) Clans(ai (19:>l). Even 
evolutionary (diange among (dos(dy related lineages of within Individual genera of Madllnae, processes of 



r\ (diange and the Biological propcrlic: 

a1 ur( 

s o 


Volume 93, Number 1 



Clausen, Keck, and Hiesey Revisited 





k p 

I ri t- 




























Kaua'i, O'ahu 
or Maui Nui - 



W T D 

Maui Nu 

DorW S 



k ■- 


*■ 5..: 













Maui Nui or Hawai'i 

h'iiniic 2o. Continued. 

linccH^rs may differ lireally. Tlicsc rcsulls miderscoiv was url! appreciated by Clausen (1951: 29-30): "It is 
ihc value of j)liylogcnclic data in pmcess-orientcd 

now established as a "ciicral hiologicaJ law 

1 Icl 


evohilionary slLuhes and llie iinporlanre of pliyh)ge- species that occupy many kinds of environment are 

nctic considerations in classiCieation at all levels of able to do so because they have evolved series of 

evolutionary divergence. physiologically distinct races, each of which survives 

A recurrin- finding in die re-examination of within its native zone but is less able to compete ni 

larueed evoluliuii using 


eru systematic ap- 


1 usual] 

proaches lias been tbe disc()\<M-y of cryptic- or senii- 
cryplie diversity, even in groujts that were studied 
iuUnisivelv by Clausen, Keck, and lliesey from an 
experimental biosystemallc persi>eclive (e.g., Layia). appearance of the plant. Ecological races or ecoLypes 

neignnoruig zones aTid ustiaiiy is imablc to survive ni 
the extreme ranges of the species. This fitness is 
primarily physiological; it is (h-termined by genes, and 

not I)e expn^ssed in the external 

It tnav or may 

Tn part, such diversity appears to reflect ecologically 
differenlialed and evolulionaiily divergent — though 
oUcn iulerfertile — lineages, as in L pallia alio ides. 

Similar exain|)les 

ular plulogenetic and ecological studies of other plant 

liav(^ ihcrefore generally been ov(Mlooked by taxono- 
Miists, geuetic-ists, and ecologisls, all of whom looked 
for visible characters llial ihey could classify. 

les have emf^-^^ed i-eeently from molec- Actually, however, the ecological race is a far more 

important biological enlily dian the morphological 

laxa that were a focus of previous e\p(M-imeulal work. subspecies. 


sucn as 

Laslhenia Cass. (OnuUiff, 1966; Chan el ah, 
2002; Rajakaruna et ah, 2003). The potential 
hnporlatice of ecologically ihsiiuet, cryptic groups pos 

' Altlunigh infeasible during Clausen's 
\\{\\ resolviim ''ecological races" that correspond to 



f ta^ 

natural groups wortli) o! laxonomic i-ec,ognilion is no\\ 



and desirable, especially in light of die 


Annals of the 

Missouri Botanical Garden 








K. bolanderi 509 

C. muirii 618 

A. scabridus 676 
A. madfoldes 488 

W. gymnoxiphium 76.022 

D. laiifolia B675 
D. paleata 1375 

D. raillardioides 670 
D. menziesii 522 
D. reticulata 664 
D. arborea 527 
D. scabra I. 778 
D. ciliolata c. 529 
D. ciliolata g. 659 
D. herbstobatae 1244 




D. sherffiana 515 
D. laevigata 671 

D. imbricata 667 

D. plantaginea p. 1180 

D. plantaginea h. 1183 

D. plantaginea"B\-\'' 776 
D. microcephala 1044 

D. laxa I. 662 

D. laxa h. 833 

D. pauciflorula 668 

D. knudsenii k. 1047 
D. knudsenii n. 1322 
A. callgtnis 680 

A. sandwicense s. 657 















Fi-iiiT 26. A pliNlogciu'lic hyiM.tlirsis ((.iic of four iiinxi. nail) parsinioiiuju^ iirr^) lor iHTcnnial n.,^inl..M-s n{ \hr "Madia"' 

]inra<^(\ w itli liinc-calihralcil 

laiiclu's. hasrd on uurU-Av l\^\\ ITS scqiuaice^ (a.lapU'd fiotn liaM^Mii cK Sandor^on IWM) 
(.onlnu-nlal larur.-ds (Anisorarpus. Car!<iiu.siia K C. Balduin. an<l Kyhosiu) and the llauaiian silvorsuord allianc-o 
{^\rgymxiplnunu Puhautia. and II ilLrsm) urr.' incdudrd n, d,r analysis, d1u- ont<,n-o,i|. (/Ulcm^llnnnnus valtdus and RaillardeUa 
prniiilei) is not shown. Kato-conslancy of tiiolocular evolnlion across linra-os r-ould nol he ve]iH-\Pi\ nsin- FrIs.awl.-inV [WW]) 
likriihood-ral,.. lost: l.ran. I, lon^d.> uorr opiin.i/ed to cMiforni lo clork-like e\o]nlion U-sin- MMxinMnn-IikoMhood Kxlornal 

talilaalion of tlu- 



n 01 ttu- n.Hio re()rc.scnlin- Ih.^ most recent ooiiHMon anrrstor of the rontin.-nla! peRMinials and llio 1 lauaiian tava uas 
on [\w assnniplion thai dl^o^si^(■ation ahnvv thai nod(; wonid not have oerunvd nntil aflcr niid-Mioconc 
(If) nnilion ycais ago), wlirn siiniincr prrri[.ilalion in U(-stern North A 
tarwords arc restrict. -d t(j areas of sninrncr-dry cliniato; sec Hahluin 
al)l)rv\ ialion^ of ^nhsfjccies in Duhaulia. 

tnerica hc<i;an to tiecline (nearK all ennlincntal 

.K S. 

md<-rMin, ]99{>). See Fiiznre 27^ caplifui \\w 

Volume 93, Number 1 


Clausen, Keck, and Hiesey Revisited 



Fio-m-o '^7 Crossing. Iiagram Rhowing svTillH'lic and natura] hvI>ri(U hclwcci species oC diUcnail life-form in ll.e llauaiian 
.,lver.wnnl allianee l»as<Mi on data of Carr (1985) and Carr and K>l.os (19[J1, 1986). Crosses in all allempled eomlnnalions 
weir .ueees.fu] and vield.^d livhrids of al l<-ast partial fertility. lieprinled from Carr et a1. (1989) u.lh permission of die 

pnhlislier, Oxford I niversit\ Press. 

polciiLial evolulioiiaiy i!n[K)ftance of sucli litu^ages in 
ihe face of rapid global change. An Ini|>ortant 
eliallenge in the eoniing years for sysleinalists \v(nkin 

of ni()h;cuUir phylogenetic methods has created 

alnahle framework for integrative sytilematic 


an niv 

stuches of yonng lineages. 

Recent metnonoioti;! 


in well-studied, threal(Mied floras, sneh as ihe a.haiiees in systematu:s 






)e to 



resolve ecoiogicaii\ 



niation of divergence 

diat aUow rigorous esti- 
times and diversific:atioii 

significant, overh)oked diversity through application 
of molecular phyh)gen(nlc and e\[)crim( ntal ap- 
proaches, much in llu; sjMrit of Clausen, Kr( k. and 
lliesey's classic invcstigalions (see Baldwin. 2()()()). 

lah's ami llie explosive growth in comparative 
iTiediods have much potential to aid systeniatisls in 
taking ph)logenetic liypolheses beyond the limilalions 
of striedy pattern-based considerations and toward 



potential of modern plant syslemalics to betl( r informed conclusions about how and why 

contribute to uudtM-standing of evolutionar) [trocesses ev 

!volulioiiarv chan2;es have occurred. The promise of 


1 fi 


le divPi-.Mty is just beginning to be collaborative studic^s of plant diversification that 

realized, with exciting results (e.g.. Rieseberg. 2006 
this volume; Sakai et al, 2006 this vohnne). 

bring together the coninme( 

billed strengths of system- 

in resolving 

Spectacular progress by systematists 

higher-level plant ndalionships through ap|)lication 

atisis, ecologists, and genetici>ls, so wed demonstrat- 
ed bv Clausen, Keck, and Hiesey, has never beim 



Annals of the 

Missouri Botanical Garden 

I JlrriilLiic CiU'tl 

AiultVcisciK K. iK 1^ (;. Rahlwin. 2{)()1. Unctuial ('\ olutionnn 
laU'.s Ik-Iuccii annual and prrmnia] lincati^rs of (.■Jicckci- 
niallows {Sidalcra, Malvaceae): Kvidcncc Ironi 1 P)S-26S 
rD.NA inlci-na! and t-\lciiial liansn-ihed spa^MTs. Molcc. 

Iiii)i. Kvol. 18: <);U)-y44. 

H^du-fH-k. R. R. lK^ II. M. Hall. M>2d-. ifemizimia congcs/a: A 
^iMiclic. ecoloiiif. and laxnnoniir >tudy of llic liaN-lu-kl 
larwcrds. rniv. Calif. Puhl. \\n{. I'A: lo-IOd. 

Balduiru P.. G. 1992. Pli) lop'iu-lic tililily of dit^ intrrnal 
trans(.Til)<-d spacers of iiiudcar rijjusonud DNA in plants: 
An fxaniplc frnin di*^ Conipu.-ilac. Molt'c. Plnlo^cn. lAnl. 
J: 'A-\fx 

. 199(>. I'll) In^f-nctirs (tl die Califoiina larueeds and 

die Hawaiian silvcrsword alliance (Madiinac: f Irliandicac 
scnsu J(iio). Tp- :r7-:^9l m I\ J. \. Hind .^ H. Beenlje 

(cdilors). ConijK)>ilaf: S)slcinaUrs. Pioccrdinu's of die 
liilrrnanniial (;o!n[)o>dac Confeivnrr, Kcu. 1991, \ ol. I. 
Royal Bii(aiiic (iardens, K(M\ . 

. 1997. .Vdapdve ra<lialion of the Hawaiian silver- 

sword alliaiiee: (^oniinienee and conniel of pli\ [oocnelie 
e\ ideiK'e from juoleeular and non-inoleeular irnesti^a- 
lions. [>p. 1()3-12[! in T. j. Giv.nsh .^ K. j. Syl.sma 
(e<lilors), Moleeidar K\olnlioii and AtlapUAe Kadialion. 
(^ainl)iid^e LIniv. Press, (^atnlnidge. 

. 1998. Fvohilion in die endeniie Hawaiian Conipo^- 

Ilae. Pp. 19-?;^ ifi T. F. Stnessv (*^ VI. One (edilorsj. 
Kvolnlion and Speeialion of Island Planls. Canihrid-e 

I _ : 1 1 i'"' I - I 

Uni\'. Press, Caniliridf^e. 

■. 2000 



and eon<fM"\'ation 

|)lanl s\>lenia[ie.s in 

(J!seo\ er\ 

Madrono 17: 219-229. 


n[ fin(^-seal(^ hiodi\(a>.Il\'. 

. 200.3a. A pli\ lo^H'nelie perspective on iIk' origin an<! 

evolnlion of iVladiinae. Pp. 19:5-228 /// S. CarKimst. H. C. 
IJaldwin X G. H. Garr (editors). Tarweeds iK- Sil\< 
Kvolution of die Madilnae ( \sleraeeae). Mi-soini BoUin- 
leal Garden Pi-ess, St. Louis. 

. 200.31). Nalnial history (if the eontinenlal larweeds 

and die Hawaiian 


\ei-svvor(l alliance ( Asleraeeae- 

Ma.lilnae). P]). I-IO //; S. Clarhinist. B. G. Baldwin X {,. 
I). Garr (editors). Tarweeds lK Silver.^words: R\(.lnhon of 
ihe Madiinae (Asteraeeae). Missouri Botanical (harden 
Piess. Si. Louis. 

-. 2003e. (di.iraclerislies atid di\'ersil\ of Madiinae. 

Pj). 17-52 ui S. Carl(|uis[. B. G. Baldwin iK (;. D. Garr 

((nlitors). Tarweed> & Sil\ erswords: Kvcdnlion 

ol llic 

Madiinae GAsteraeeae). Misstmri BoLain'cal (iardeii Press. 
Si. I.onis. 

. 20{).'"x Origin of die serfjeiil ine-en<lernie herli Li)\ii! 

(lisaiidcii fitan the widespread /.. i^hiiKhtlosa 1 ( jinipositae). 

Fvidntion 39: 2173-2 179. 

iK IG 11. Ilohichaux. 1993. Ilislorical hioi^*^ 


ecology of die Hawaiian siKcrswoj-d adiance 
( A^leraeeae): Ne\\ inoleeular- plu logeuelic pers])eeti\es. 

Pp. 239-287 in W . L. Wagner .K W V_ Innk (editors). 

Hawaiian Bioge(.g]aph\ : F\olnlion on a Hot Spot 
Areliipelago. Snndisonian luslilnlion Pi'ess, Washington 


^K M . .1 . Sa 1 1 1 lerso [ i . 

di\(M->ilicati(ai of tlie I L 

1098. Age 



1 1 


jwaiian sii\ erswofd alliance 
(Goinposil;ie). Proe. \all. Aead. Sci. G.S. \. 93: 9102- 

I). W. Kxhos i.K j. Dvorak. 1990. Gldon.piasl \)\\ 

e\olntion and atlapli\e radiali(»n in the Hawaiian silv<-r- 
swoul alliance ( A>hMaceac-Mailiinae). Ami. Missouii Bo|. 
(;ard. 77: 96- 100. 

D N A 


^ <!< C. n. Garr, 1991. GhloroplaM 

(or a .North Auiei-jcan ori'^in of the 
Hawaiian sil\ersword alliance (Asteraeeae: Madiinae). 
Proc. ,\atl. Aead. Sci. G.S. \. 88; I8> 10-18 13. 
Barrier, \].. B. G. Bahlwin. K. II. liohiehanx r^^ M. 0. 
Punigganan. 1999. Inlers])ccific h) hrld aneesli) of a [.lanl 
ada|tli\c radiation: Allopolyplold\ of the Hawaiian siher- 
swokI alliance (Asleiaceae) inferred from floral honieotie 
gene duftllcation-.. Mi.lee. Biol. Kvol. 10: 1103-1113. 

Bartort, \. 11. ^K B. GharK^worlh. 1981. Genetic re\olulioiis. 
fniMider effeels, and spi^ciali.Mi. Annual ]{ev. flci.l. S\st. 
13: 133-104. 

Garawav. V.. G. D. Garr ;K G. W. Mordcn. 2001. \ssessiueiil 
uf InLridi/.atiun and introgression in la\ a-eoloni/iu'^ 
Hawaiian Duhiiulin (Ast<aaeeac: Madiinae) usinn- RAPD 
markers. \mer. J. Bot. 88: 1088-1691. 

Carl(|insl. S. 1957. I.(^if anatomy and untogen\ in Anryro^ 
xiphiiini and W ilLcsin. \mer. J. B()l. II: 696-703. 



. 1939a. Cdandiilar stniclures of /yrj/orf/r/j/f*-/ and their 

ontogeny. Amer. J. Bol. 16: 300-308. 

. 19391). Slntlies on Madina<': Anal(tm\. c\ IoIojin. i 

evohitionar} ndalionshijjs. Ali^o 4: l7l-2.">6. 
. 1903. I>lan( 


Life, \alural lli>toi-) I', \ew York. 
. 19. 1. Island Biology, (.lolutiil )ia Lni\. Press, New 


. P.'80. Llawaii. a \atural llislor\: fieolo^iv. (iliniale. 

\ali\e Flora and Fauna al)o\e the Shoreline, 2iid ed. 
Pacific Tropical Botanical (^irdcn, Lawai. 
, B. (;. Baldwin cK G, I). Garr (etiitors). 2003. Tar- 
weeds & Silv(M-swords: F\olulion of tin 



(Aslerae<'ae). Mi.ssouti Botaiileal (harden Press. St. 1. 

Garr, G. I). 1983. Monograpii of llie Hawaiian Madiinae 

(Asteraeeae): Arg)m\ij>hiiun, Dtihamin. and W ilkesin, 
Allerloina 4: 1-123. 

' — -. 1993. A fully (eride intcrgeneric li}ltrid dcri\ati\e 

(roin \r!^\n)xii)hii(fn 
IJtiluailia nicnzic.sii 
plant exoluliou h\ I 
82: 1371-1381. 

s<in<hri((>!\se ssp. fn<icron'p}}<i!um X 
(.Asleraeeae) and its relevance to 
ic Hawaiian Islands. Aniei". J. Bot. 

. 1998. GhromosoiiK^ e\ohitioii and speeialion in 

Hawaiian (litwering phnils. Pj). 3-d7 if} T. V. Sli!e^<;- c^- M. 
Ono (ediloi>). Fvolntioii and Speeialion of Island Planls. 

Canihiidge Uni\. Press, Gainhiidge. 

.2003a. ll)lM-idi/ation in Madiinae. Pp. 79-101 /// S. 

Gar!(]uisl. B. G. Baldwin i.K G. I). Garr (editors), TaiweeiG 

tV Si!\ersword>: Fvf)lMtion of die Madiinae f \-l<'rae(\ie). 
Mis.-onri Botanical Gard.'u Press, St. Louis. 

. 2003L. Gluoiiiosome e\(jlntioii in Madiinae. Pp. 33- 

78 /■// S. Garh|nisu B. G. Baldwin <!( G. D, Gair (editors). 

lai-weeds c^' Sil\ erswords: Fvohidori of the Madiinac 
(Asteraeeae). Missouri Botanical Garden Press. S|. LoLiis. 

I.K I). \\ . K\h(ts. 1981. Adaplivp radtalion in the 

Hawaiian sil\er-sword alliance' (GompiKsitae-Madiinae). L 
C\logeneties of sponlaneoirs liyjuids. E\olution 33: 


& ■ 10[J6. \dapli\e radiation in the Hawaiian 

sil\ersw)trd alliance (Goniposilae-Madiinae). 11. (Aloge- 
nelies of arlificial and nalural hvhiids. F\oliitioii 10" 

-. B. G. Baldwni .'v 1). W. Iwhos. 199(). G\ toiicneiic 

implications of artificial li\biids hetween die Hawaiian 
sil\ersw(»rd alliance and ^orti] American larweeds 

(Asleiaceae: lielianl lieae-Madiinac). \\wv\\ J. Bol. 83: 

■ IL H. Kohichaux. M. S. W iiier lK I). \V. Kvhos. 

10rj9. \ilapti\e radial ion of the Hawaiian silversword 
alliance (Gomposilae-Madiinae): A eoiiipaiison with 

Volume 93, Number 1 


Clausen, Keck, and Hiesey Revisited 


Hawaiian picturc-w in<^(Ml Drosophihi. P\). 7*)-97 tn L. \. 
CiiMIn^s, K. Y. Katu'sliim .S. \\\ W. Andnso.i (, 
Ct.'iu'tics, Specialioii and [Up FoiindtM- Priruiplc Oxford 
Univ. Press, iNew "^ nrk. 
. B. G, Balduin <!v J. P. Slrother. 20(i:'). Ac-ceplod 


: 1990. GcMuMic sludics of floral evolution 

names and synonyms for specific and inirasjieeific la\a in 
Madiinae. Pp. 229-21:^ /;/ S. CarUiui^t, 1^. G. Halduin & 
G. D. Carr (editors), 'raru(-(HLs & Silvei'swonls: pAolulion 
of the Madiinat^ (Asleraceae). Missouri Rotauical (ianlen 

Press, St. Louis. 
Chan, K., P, G. I5aid^^in & R. Ornihiff. 2002. Cryplie 
"■oldfields: A molecular pli>logenetie re-iuvcsll^aliou of 

Laslhcnia (■alifi)n\i(<} scnsu 

lata and close relalives 

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Cla-uc, D. A. & G. p. Dalrymple. 19P,7. '\hr llavvaiian- 

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French, G. S. 1989. Jens Chri^lian GlaUM-n: March 11, 1891- 
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38: 7.'>-95. 

GiNuish, 'U J., E. Knox, T. P. Patterson. J. D. Palm(M-.^ K.J. 
Sylsma. 1996. The Hawaiian lohelioids are moiioph\]elic 
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Goltlitd), U, D. 1973. Genetic diff.M-enlialion, sympalrie 
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, S. I. Wanvick & V. S. Kord. 1983. Mor[)liological 

Fuipcror volcanic chain. Pp. 1-34 in \\. W. Dcckei-. T. L. 
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S. (ieolosieal Survey Professional Paper 1330. U. S. 
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Clausen. J. 193U Slag(.'s in the evolution of plant species. 
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and eleclrophorctic divergiMiee hf.'tween Layid (liscoidcd 
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Grant, V. 1963. Tlie Origin of Adaptations. Colnmhia Univ. 

Press, New York. 
. 1971. Plant Speciation. Cohimhia Univ. Prrss. New 

^ ork. 
™. 1981. Plant Spccialion, 2iid ed. Columbia L uiv. 

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, D. D. Keck & W. M. Hiesey. 1939. TUr concept of 

& . 1940. Experimental Studies on 

the Nature of Species. 1. I^ffect of Varied l-^iu ironmcnts on 
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Carnegie Inslitulion of Washington Year Rook no. 40: 


. 1943. Experinieulal Studies on 

the Nature of Species. II. Plant Evolution through 
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and eeoloRicallv isolated races. American 

. I947. Heredity of geogra])hically 

Naturalist 81: 


AiniM-. Acad. Arts 2: 139-100. 
Hall, II. M. 1932. Heredity and environuKMil — as illustrated 

by transplant studies. Sei. Monllil) 33(October): 289-302. 
Keek. D. I). 1936. The Hawaiian silverswords: S>sLcmatics. 

affinities, and |)hylogeograpliic [j|-ol>i(^nis ol llic genus 

Argym.xiphiuiii, Occas. Paji. Rrrnice Pauahi Bishop Mus. 

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American ultramafies. Pp. 31-73 in B. A. Roberts eK J. 

Proctor (editors). The Ecology of Areas with Sci |H-nt!ni/ed 

Rocks: A World Vdew. Kluwer Academic Publi>hcrs, 


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. 2002. Geology aru 


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Kvhos, 1). W., G. D. Carr .^ P. G. Baldwin. 1990. 
Biodiv<-rsily and cytogenetics of tlic larweeds (Asleraceae: 
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Evolution 48: 19-30. 
Grins, W. J.. B. A. P>olmi l^ G. D. Carr. 1988. Ela\onoids as 
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the exception. Syst. Bot. 18: 1.97-208. 
Lewds, 11. 1966. Spccialion in novscring plants. Science l.:>2: 

& M. R. Roberts. 1936. The origin of Clarkia 

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conee[)l and recoumioudations for a pli) logemnic alterna- 
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Ehrli(Ji. P. R. & P. II. Ra\<'Ti. 1969. Hiircrentiation of 
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Eelscnsteiu. J. 1988. Pli\logeuies from molecidar s<'(iuenees: 
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. 2004. Infcrriiifr Ph\ hi^^enies. Sinauer Associates, 

Ford. V. S. & r.. D. Gottlieb. 1989. Moi-jthological evolution 

methods and the geography of speciation. Trends Ecol. 

Evol. 18: 220-227, 
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R. Eiss, New York. 
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E.vohilion 33: 66)1—668. 
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ni"//;r/V/(Compositac]:Charact(M- recombination in hybrids Ornduff, R. 1966. A biosyslematic survey ..f tlic goldficld 

genus (.asthenia (Comj^osilac: Helenieae). Univ. Calil. 

between L discoidca and L ^laiiduh>sa. Syst. Pot. 14: 


Publ. Pol. 40: 1-92. 


Annals of the 

Missouri Botanical Garden 

Osboiii, ]l. F. ][)i)2. Thr law ora(lapli\c radialioii. Aiiirr. 
Naliiralisl 'Mr. lirvA-Mhl. 

Palnirr, \l. K. 1982. l\(H)l()'ii(-al ciinl Evfyliilionarv [^itlciris in 

I'li.D. (liss('rtalic>n, IJtilvcrsih of CalifoMiia. 

I)a\ Is. 

, 19<>7. E\()liiti(Miar}' rehitinn>lii|)s of ILdiH'tirplui 

29r)-:](M- in T. S. Elias (.Mlllor). 

CoiisciA al 11)11 




lodan^crcd IManls. 



fNal r\(^ 

uirc arm 
Plaiil SocirLy, 

Rajakaiiina, \., \]. {], iSaldwtn. R. riiati. \. M. Df.snjcli(M-s. 
B. '\. !^)liiit .'^- J. Wliidon. 20();5. Kdaphic rarcs and 
phylop;*'n('lir laxti in Hie Ldsllie/iid califonnca (A^^tcraccac) 
coniplrx: An hypollicsis of parallel rvoliilioii. MoK-c. Im-ii1. 
12: If)7r>-I679. 

rui\i'ii. \\ II. lK I). I. Axrlr.MJ. I97P). ()ii,u[n and i-olalioii^liips 
ol llir Califuniia floia. rniv. Calif. Puhl. HtA. 72: I- 


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Ann. Missouri Rot. (;ard. <M: .34-^UJ. 
c'^ L. Hrf>rnil('l. 1994. Are many planl sjK'(i(\s 

para[)li\ Irlir? Taxon 1."^: 2I-.H2. 
cK J. M. Rnrke. 2001. Tlr( 

)io o^ica 

i'<'alil\ ol 

spooics; (a'hc f\i>\\\ s('l<M'lion, and concclivp evoliili4)n. 
Taxon aO: 17-67. 

Hohioharrx, K. II., G. 0. Can". M. Liol.nran (K K. \\'. IVarcv. 
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allianci; (( :(>nipositar: Mailiinae): KeologieaK rnorpliolo^i- 

eal. and |")h}sioio^ica 

li\ersil>. Ann. Missoirri liol. Card. 

77: <)l-72. 

Sakai, A. K., S. (J. WVIIer-. W. p. Wagner. M. Nepokrocff & T. 
l\L (adiey. 200(t. Adapti\e railialiim and e\(tlntion of 

S( Inedcd M lar) oplixllaceae). an 

hree[lrn<i .^)^,tcins m 

endrtnie Hawaiian '-enirs. Ann. Mi.ssoin-i \]n\. Ciml. 9-']: 


lai- Selilnler, I). 2000, Tin 

LroKjgv of 

Adaptive IJadialiorr. 

Oxford Univ. Pi'ess, ()\fo|-(k 
Sinipsofi. (;. C. 1911. T(Mnp() and 
Cniinirl>ia I niv. I^i-ess. Nenv York. 

Mode in F\olntIon. 

. 1953. The Major Fealnres of lA oiniii.n. (iohiniliia 

Unix . I'l-ess, .New ^'or■k. 
Slel)liins. (;. F. 191-9. Itate.s of cvolnlion in ])lanls. Pp. 229- 
212 m (;. L. JepsiMi, K, Mayr X (,. (]. Simpson (rditofv). 
Cerrrlics. Paleontolog), and F\olulioii. Prineelon ld)iv. 
Press. Pi-incelo!]. 

. 1966. Prdeesses of nr-gain'c cvolnlion. Preirliee-I lall. 

I'ai^lewood (Jiffs. 

. 19r,2. Planl specialion. Pp. 21-39 /// C. nan<;o/,/i 

(editor). Meelranistns of Spe(dation. Alan ]\. I.iss. New 

riiornas, K. H. .K J. A. llmil. 1991. Tl.r molecular evolirti 


o( the alcohol deh) dr-o<:;enasc locus and the pli\lo^(ai) of 

Hawaiian Dmsophlla. MoFm'. Hic^i. fAol. 8: 687-702. 
Warwick. S. I. ^K P. I). Coulich. |98o. Ccnciic di\.M-gence 
and ^('oiir-aphic specialion in Litvid (( -niniiosilae). P\olu- 
liorr. 39: 1236-12 11. 

Volume 93, Number 1 


Clausen, Keck, and Hiesey Revisited 


](' rigui'cs 

Ai'i'i:\l)l\ 1. Auiliorilics for spct:i{\s [)rcsenlcu in 1 
wlu'ii ull](.'r\ nol prt)\ idcd iti tho lexl. For a cotTiplcte 
listing of acfoplfMi names and synonvms for spcciric and 
infraspofific taxa in Aladiniiae, see Carr et al.. 200'^ 

AchyRtcJuiena mollis Scliaucr 
Ar^yroxipltium ralignis C. N. Forbes 
Argyroxipbiiim gr<n<iniiiu (I lillcbr.) (). Deg, 
Argvroxlphiuni kdncnse (lun-k & M. Neal) 0. Dcg. & T. 

fjlcpliaripuppus scaher Hook. 

Hlephdrizonid lax<f Chmmu' 

(Ailvcrnlrnia fmnnntii A. (iray 

Ceiilronuidui perenfiis Greene 

Dclnandni greciivdna (Kose) B. G. Bald\\in 

Diibdulia arhorcd (A. Gray) D. I). Keek 

Duhdiitid hcrh.sldhdldc (]. I). Carr 

Diihaulid imhricdld W. Si. John & C I). Carr 

Duhdiilui laeL'igala \. Gray 

Dubdutid uilci'ucephdhi SkoLlslj. 

Dulxnilid pdlcdta A. Gray 

Dtibdnlid pduriflnnila H. St. .|i>lin & G. D. Carr 
Diibdiilid pldtvphyUa (A. Gray) 1). D. Keck 
Diibduild idilldViUoldes Ilillehr. 
Dubdulid shcrfflana Fosljcr 
Uarmonld slcbhinsii (T. W. Nelson .K .]. P. Nelson) H. G 

JleniiZduid congestd DC. 

lloluzonla jlUpes (Hook. & Arn.) Greene 

Lagopliylld niiiior (D. D. Keek) I). I). Keck 
Ldvld hclcrdfricbd (DC.) Hook. S: Arn. 
Miidld alriddord Greene 
Madia exigua (Sni.) A. Gray 

Madia glouu'rahi Hook. 

Madid gracilis (Sni.) D. D. Keck lK J. C. Clausen ex 


l\1ddid radidla Kellogg 
Mddia subspicdla D. L). Kt'ck 
Osnuidcnld Icnclla NiiU. 
Wilkcsid liobdvi H. St. John 


Peter R. Gnml/ and B, Rosenidrr (WdDl' 


The .Kla|)ti\r radiation of Darwin's riiulies in I he Galapa^tiiis nrrlii|i*'!a,i;<) slands as a tnodtd of spccios niiiltiplicahon. Tin- 
radialioii Lr^an two It) lliree million }cais a^o, and ivsnllcd in II s|)(H'ics hcin^ derived Ironi llie oriii,iriaI eoloni/iniz; species. 
Tins sysleni is lii^lils snilahle fur invest igaling die eanses ofspeeiation Ijeeause closely relaU^I ^jjceies occur s) in[)a[ricallv in 
se\'eral eomhinations and in en\ ironinenis willi r(dati\el} litllc anlliro]K»geni<- di.slnrhancc. Tin; loje of natin-al ^election and 
adaptation lo ieediim niches in tlu' al]opati-i<- phase of special ion has been detnon si rated )-epeal(M||\ . In the sytnpatiic phase of 
speeialion, difrercnces in son^ and morphology act as a premaling barrier to ji;ene exchan^i^e. This form ol reprodncti\e isohition 
c\ oKcs at leasl parll\ as a passive cons(xnicnce ov hyprothict of adapt i\'e diviM'^ence in Ix-ak niorpholo-;) . Son^^ cliaiaelei'islic.s 
(h'vergf^ in adopatry. largely independent of beak tnorplutlogy ami for a variety of rea>(>n.-, not all of which are uell nntlerslood. 

'il)c barrier lo gene exchange in s\rnpal!-v is nol eornph-tcjy effective, however; spiM'ies hyl)ri(h/e rand\, and nnder ^otnc 

cirtaimstances the h)bnds aie Mn]irisingl) lit. These ic-^nlts challenge some cnrrenl notions of species. For e\am])le. die 

l^romid linch species Geosplzd scdndcns Conld and G. for! is Gould on \W island of f)a{)hne Major have lost morphological 

diagnosability, as a result ol inlrt)gressi\ c hybrith/ation, while retaining \oca1 diagnosabilit) . Speeialion is n process of 


divergence, and tluM-efore lh(^se two population^ avc currently despecialing. With a change in clijiiatic conihlions ihey an 
expected to respeciate. Snch mergi^-and-di\ ei'ge dynanncs m;i\ oc(an" fretpientK 


1 tnnnc] 7ones :ni(i ni rei;ni\(M\ \ounii 

radiations In habitats subject to strong en\ iionmcntal fhiclnations. 

Key words: allopatric divergence, c-onservatiou, cvolulionary |)otential, hybiid filncss. imprinting, introgre.ssion, song, 
s|)ecies bai'rier. sp(M'i(\s eoncejjt. 

Two inler-rcdalrd (jueslions in evoluliotiary l>i()l<)gy radiation. (.)iie k(^y coniponcnl is adaptive (II\(a-g(MKa 

lia\<' l)een discu^stal inleiisi\(d\ in llu^ last decade. 

\n rcriource (food) (^\j)loiting trails. Tlirec major lines 

These are: what are species, and what role does of e\idenee denionslrale the role of natin-al selection 

liyhridi/alion |-)lay in speeialion? '[Uc dehale a])oitt in divergxaiee (\\ W. (xrant c'^^ H. K. Grant, 1997a). 

sj)e<des is alxnil eoneepis and <aileria (('oyne iK Orr. FirsI, po[)u]ations differ ecologically on different 

20(11; do Ouriroz, 1998, 2()()(); Harrison, 1998; Hey, islands that ba\<' different arrays of food resources 

2001: Mayr, 2000. 2001; Orr, 2001; Sbau, 2001; Wiu (Abbolt d al., 1977; SmiUi et al'., 1978). Second, ihe 

2()0la, I)), ddic d(diate ahoni h) bridi/atioii cejiLers on parli(adar sp(Hdes on an island and tlndi- iK^ak sizes 

ulietlun- it has a creative role In s])ccialion throngh are predictaldc lo a large extent from the food snpplv 

enhancement of mullilociis genetic \-ariation, or (Schlulcr & Graiil, 1981). ddii rd. wlien the food 


Boag & 

hcther it has no cllecl or even relards or reverses envii-onment changes, evohitionary chang<' occnrs as 

the process (Mayr, 1942; Sl(d>hins, 1930; Svaixlson, a result of natural sideclion on heritahh^ variation in 

1970; Metdiatn, 1975; Ra\cn. 1976; Arnohl. 1997: beak si/c and slia|>e as \v(dl as bodv si/. 

Hercus & Honmatni. 1999; Rarrier et ah, 2001; Grant, 1981: B. li. GranI iR \\ \{. Grant, 1989; P. R. 

Barton, 2001; Mailinsen el ah. 2001; Ortiz-Barrientos Grant X 8. R. Grant. 1993, 2002a). 
el ah. 2002: Rieseherg et ah, 2003). The two suhjecls A second key cbm])oncnt is di\ergence in eourtshiii 

are inter-ndalcd because ulieii |n)pLdalions ]i\hridi/.(\ signals and responses leading to rej)i-odiicli\ e 

and therefore aiVMiot complelcl) i.'^olale(] icprodnctively latioii of two populations d(M'i\'ed from on(\ ddus is tlu^ 

from each otiier, the (juestion arises as lo whelhei- tbc) focus of our arti(de. Wc address four (luestlous: whal 
should he considered as one species or Iwo. 

We address ihc two issues of s|>ecies and related sj^fxdes, liow does it originate, liow nnghl it Ik 


constitnlcs a harrier lo <ren(^ excdianiie helween (doselv 



)rKli/atioii I)y discussing icc(mU finding.> from field 

breached, and whal are the consecjnences of oeea- 
stndi(\s of Darwin's liii(dies on ihe Gala[tagos islands. sional hybridi/at ion? Answers lo these (inestions 
The stndies arc d(\signed to iiut'stigale the causes of (.■ou^.lilnte tlie ba(dxground to a comdudiiig discussion 
sp<^ciati(tn within tlic broader context of an adaptive o 

f s[)e(des as laxonomu- uinls. 

Onr research has bee 

f tl 

» t 

n earned ont uuiU'V the auspices of the Scrv icio Parcpie Xaclunal (Galapagos, CharU\s IJarwin 
Foundation, and Fhadi^s Darwin fb-seardi Stati(tn. ft has l)een sujiported bv ffvsearcli grants Irom \SF1U^ ((Canada) an.! \SF 
(L.S.A.). We ihank ihe numeron^^ assistants who luni- hel()ed with fn-ldwork. HsUmI in ])revi<tns publications. 

^Dcpaitment of l''eolug\ and I\\ olnttonnrv I'lology. I'rinccton Univ (-isily, Princehin, New Jersev 01)3 1 1-100?). U.S.A. 

A\N. Mis.^()ii8 Bor. Gaki). 93: 94-102. Puntsiiid) ()\ 81 May 2006. 

Volume 93, Number 1 

Grant & Grant 


Tmk Rvhkikhto Gkni: K\{:ll\^(:E and init morphology, and coiise(|uently hybridize and 

prodiUH^ liyhrid offspring. I( ihey are males, they siti^ 

Darwin's finch species are sinular in ihe lype of the same single song as sun^ hy iheir fathers and male 

nest ihey build and, as far as we can icIL in iheir ■^vitli a female w^iose father sang that song type (P. I{. 

courtship behavior (Lack, 1947; Ratcliffe <.K Grant, Grant c^ B. K. Grant, 1997c). If they are females, ihey 

1983a). Species in the same genera are similar in clioose a male that sings the sanu^ song as theii' fathers'. 

phnnage but differ in heak morphology and song (P. R. Even though F| hybrids and hackcrosses are morpho- 

Grant, 1999). Dinei-ences in these latter two traits l(j<ilcall> iiiiermediate between the parental species. 

wonhl appear to be ihe best candidates for harriei's to tl^ey breed strictly according tn song t\|)e (B. \{. GranI 

gene exchange and, indeed, field expei-iinents with S. P. R. Grant, 1998). Thus, ihroLigh occ-asional 

syn][)atric sj^ecies in ihe ground finch genu^ Ccospiza niisimprinling. introgression of genes occurs in Ixtth 

Gould have confirmed iheir potential roh-' (Hatclilfe & directions between Geospiza forlis and G. scandeiis. 
GranU 198;ia, 1985). 

H^iJini) FiTM'.ss 

Hybrids ha\e been formf^I rartdy (-^1% of brecihug 

The two sets of trails ai"e interestingly (Hnerenl. beak 
size and body si/e are polygenic traits that (hsplay high 
herilahililies (P. R. GranI & B. R. Grant, 2()00; Keller 
el ah, 2001), whereas songs, sung only by males, are paii's are inters])ecific), but approximately contiiuious- 
cnhm'aM) Iransmitted fro!n father to son (B. R. (irant & ]y. ihroughout our 30-vear sludy on Daplnie Major. 
1^. I{. (^rant, 1996a). Bowman (1983) demonstrated with How(wcr, in (he first 10 years none survived U) hiced. 
lab experiments that songs of Darwin's (incht^s are At ihis time we considered two possible reasons for 

learned, in an imprinting-like manner, helvveen their failure: genetic incompalibihty and ecoh)gical 

aj)[wo\imateIy day U) and da> 30 after hatching. These insuffici<'ncv. Few birds, hyl)rids and non-hybrI(Ls, 

20 fhiys cover the pei-iod from the last few^ days in ihe sin\ i\('d the generally poor feeding conihtions in the 

nest to the end of tlie fledglings' dependence on their carlv vears. H)brids, AVilh their intennechate beak 

parenls. The fallier sings lln-onghout this time. Our field sizes, wcv^ unable to crack the large and hard seeds 

sliuhes support Bowman's laboratoiy fin(hngs (B. R. of Trihiilus cisloules (L.) thai the more robust-l)ilhMl 

Grant cl I^. R. GranU 1989; Gibbs, 1990). They hliow Ccospiza fortis were feecHng on, arid they look 

that a strong resemhhnice exists between song significanlly longer to crack open the seeds ol Opunhd 

characleristies of sons and ialhers and even paternal eclnos Mowclb which is the main dry-season food ot G. 

grandfathers but not TTialei-nal grandfathers (B. R. (»ranl scfirHlcns (B. K. Grant & P. B. Grant. 19961)). After the 

& P. R. (;rant, 1996a). 

Ofleu exception 

s are more revealing than the inle. 

unjirecedcnledl) high rainlall in the Fd Nino year of 
1983. the ecological conditions on ihe island changed 

lm|)rint(Hl traits, being learned, are snbjcM-t lo mis- dramatical!} (P. R. Grant et al., 2000b). The pre\iously 

imprinling if young birds are exposed to the song of common large and hard seeds (jI T, cisloides and 0. 

a (hfferent species ralhcr than, or more ihan, the echios diminished in the seed hank, these plants having 

lather's song, during the short sensitive i)erIod of been smoduM'ed by vines and other small-se^Ml [»ro- 
learning. This has been obser\ed in a stud\ ol Geospiza 
fortis Gould (medium ground finch) and G. scondens 

ducing plants. Under these altered conditions ol an 


umdance o 

f small and sofi seeds, hvhrids and 

Gouhl (cactus finch) on ihe small island of Daphne jjackcrosses sur\i\ed to reproduce. Therefore, their 

Major (B. R. Graiit cK P. B. Grant, 1996a. 1998; P. B. prexious failure is attributable lo ecoh)gIcal insuffi- 

Crant & B. R. Grant, 19971)). Misimprinting ha[)pens ciency and not lo genetic ineompalihility. 

rarely, in three tvi)es of carcumstances. It occurs wlu-n After 1983, hybrids survived as well as, if not better 

(1) a fatlua- dies and the offs[iring learn the song of ihe than, their jiarental species, and reproduced as well as 

nearesi natal neighbor, which can be the bird of lliem. there being no diflerence in number of eggs, 

an(ither species; (2) nests of two species are close nestling>. or ncdglings produced (P. R. Grant & B. R. 

together and one male ^ings louder, more pei'slsliaitly. Grant. 1992j. We detected no loss of litness in ihc F| 

and chases off ihe otiier male; and (3) a tiesi with one and backeross generations in terms of relatively jxior 

survival, mating success, or reproduclion (P. R. Grant 

of the original eggs in it is taken over by a [)air be- 

longing to another species, the egg hatt lies, and the & B. B. Grant, 1992; B. B. Grant & P. R. Grant, 1998; 
neslliuir isfedbv and learns the son"; of its foster father. P. B. GranI et ah. 2003; but see Barton, 2001). 

lM"[i()(;KL:ssi\K Hviuni)i/.\rtox 

PmI'LICATIUXS of I\TR0(;[n->s|()N 


owing the fates of 16 misimpiinted nntaies 

I fined 

has 'Inhere are two important implications of the 

re\ealed that they mate mainly according to song lype docunienled introgressive hybridization. First, [losl- 


Annals of the 

Missouri Botanical Garden 

tTuiling i.snlnlioti appeal's not lo liavc cvoKcd Ix-lweeii no discriininalioii Itolween an ininii^rant aiul a (rosi- 

lliose and other pairs of ground finch specic^s (B. R. dent) nienil}er of (he lespondni^ bird's own |)opLilal imi 

Grant & P. R. Craiil, 1989, 1998; W R, (^.lanl el ah, when h(\ik <hfft;ieJices between them were small, and 
2005). Ev<Mi more distanlly rehited species of 

sti'ong discrimiiialion vnIumi the (hllei'enccs were lar<;e. 

Darn ill's finches ha\(' l)een known, or suspected, to Acoustic cues were controlled for in dicse experi- 

h\bi-i(lize without a recorded loss of fitnc^ss (P. R. 
Grant, 1999). d1iis is not surj)rising. According lo 
comparalive evidence fi-om oilier bud species it lakes 

more than two niilli 


on years lor post-/)go[ic \n 

ments by (ditninaling them; dead museum >[>ecimcns 
do nol sing! 

Playback experimenis without nuiseum specitnens 
as visual cu(^s showed lliat ground fiticlies diacj'inii- 
nate acoustically between residents and immigrants in 

com|)alibUilies to evol\e (Price eK Bou\ i(M\ 2002). 

Alh or almost all. of ihe aihiplive radiation of a similar way to [heir visual diseriminalion: llu 
Dai-win's finches took place in less than tliis lime 

(P. R. Grant. 1999; Sato et ah, 2001; Burns el ah. so wIumi they are small (Ralcliffe & Grant, 1985). 
2002). SfH-ond, hybridization and backcrossing has The morphological barrier arises as a result of 

enhanced ihe evolutionary ])olcnlial of llu^se tuo adaptation. As such it conforms to an old idea dating 

discriminate when (hlferenees ar<^ large and fail to do 



s[)eeies oy increasing additi\e genetic \ariances 




wnue reducnig eonstranits Irom genetic correlations 
(P. R. Grant & B. R, (irauL 1991). Hie reduction in 
sIrfMigth (tf genetic coiTclations Ijctwecn beak size 
Iraits is due to the inl(a's[)ccific differences in 
adometries. In principle^ a ihird implication is thai 

liybrids have ihe potential lo if!\ade new habitats bif)mechanical reasons. aff(M-tini: Irill rale and tJu 

l)ack al least 65 )ears Lo r)ol)/hansk\ (1937) dial 
reproihiclive isolalion originaU^s as a bjproduci of 
ada|)ll\(' dilferentiation. We know less about how tlu^ 
song barrier arises (B. R. Grant t^ P. R. (;ranl- 2002; 
P. li. Grant & B. I{. Grant, 2()02b). One possibilit) is 
lliat song charact(M-istics covary with beak si/e f 

' \i)V 

(Lewontin i^ Birch. 1906) ami even foiin a new^ 

range of (rctjuencies ol indi\ idual nt)tcs (Podos, 1997) 

s[)ecies in another cn\ in)nnKait (see Rieseluag, 2006 and, tluMvCore, when beak si/c changes adaptively, 
this issue). We conjec:Iure that introgressive hybrid- 

songs change as a passi\(' consequtaicc. Ther(^ is 

i/alionnia\ have contributed to speciation in the past, some su|)pi)rting evidence (Podos. 2()()lj; nevcrtlu- 

allhough wc lack evidence thai this happ(Mied in any 
part icidar cas(\ 

'Vm: {)\{H'A\ iiv .\ BAtuuKKTo Ge^\: Exciia^ci-: 

less, corrclatcHl cflccts of beak change a|)j>ear to be 

insuflicicnt to set up a barrier to gene exchange 

l.)eeause coexisting sister species of (j^'ospizd do nol 

diller discretely In these two song features (B. R. 

Grant <*v P. R. (^rant, 2002). In conliast to this 

Based on these findings, reproduclive isolalion of int.a-spccific similarity, populations of the same 

Darwin's finches is explained by a theory of species may differ substanlially in songs independent 

discrimination by song in association with morphology of beak sl/e (h'fferences (P. R. (irant el ah, 2()()()a). 

dull is learned in a sexual imi)rinting-lik(^ process The hypothesis is undenuined ])v ihc ainlitv of 

early in life (B. R. Grant eK P. R. Grant. 2002: P. R. 
(;rant & B. R. Grant, 20021)). 

S}'m[)alric species w illi diflererU beak sizes to sing 
each other's sonjis with scarc(dv altered t:haracter- 

We now apply conlcmporary findings from Daphne islics (Bowman, 1983; B. R. (w'ant & P. R. Grant. 

to the c|uestion ol how repi"oducli\(' isolalion evoR'es, 

1989. 199!!: P. R. (;rant & B. R. Grant, 1997b, c). 

using as a framework tl 

^e allopatric model of Gorndatcd effects of jjod 

s oi ijoov sl/e ehang(^s may also 


conirnxiU^ lo a barrier thi'ough an inrinence on 

spccialion. The rncidel invokes ecological a(hi|)lation 
in alloj)atry as a recpiirement for the establishment of fre(]ucncy characteristics of songs (Bowman, 1983). 
sympatric coexistence of two -pecies derivcnl from Since beak size and b(»(K' si/e iicnerallv co\arv. a third, 
one. For this there Is t.)lenly of evidence (see and more realistic, hypothesis is that they are jointly 
inlroduction lo this artich^). A total oi- n<'ar-lolal hick 

invoR'cd in determiiiing charactcrislics <if songs and 

of inlerbrecding is another retjuiremenl. ITe model hence the barrier to interbreeding. An(»lhcr [possibility 
invokes an allopatric origin of a |)re-mating barrier lo is that a new song type ma\ originate as a cullLU'al 
gene exchange. KxperiuKMits show that some degree of 

mutalioti through miscopying of fallua's song and 
Increases in freinicncy b\ chance or s(dcctivelv. A 

selective advantairt 

if tl 

gc may ai'i^e il the >ongs tran>mit 

dldcrentialion in ihc cues used in mate choice must 
arise allopatricallv. 

hxj)erimeuls with museum specimens lr(Mn dil]ereut better in the new fMuIronmenI and. as a result, mon^ 

islands were conducted to sinmhile the s(H'ondary effectively rep(d Intruding males or attract females. 

contact phase of the speciation cycle (Ratcdiffe lS. The oiigiu of re]}roducti\e isolation is .-till nol fullv 

Grant. 1983b). In a variety of lests with different understood, and these possibilities need further 

ground finch sj)eeies, we consislenlly found w(^ak or investigation. 

Volume 93, Number 1 


Grant & Grant 


Ai)AFn\K l)i\i:KSiFiCATiON'riiKorGH RKPKAri:!) Speciati()N 2002; 1*. K. Grant & B. R. Graiu, 2002c). On (he 

island of Genovesa, ()c:cu|>icd l)y Certhidea fiisca 

The fuix'^olng explanatKin ol how h\(j species ai'e 

Sclater, we tested hi ids wilh their own songs, songs 

foi-mcd from one serves as a hasis for ex[)huniiig ihe fVom anolher popuhilioii of C. fusca, and songs from 

ada|)tive radiation as a whole (P. R. Grant & B. fv. two popuhilions of C. olirdcea Gould. We performed 

GranI, 2002c). fourteen species evolved from a single similar experiments with the sam(^ phiyhack tapes on 

ancestral sp(H*ies by a simple repetition of the process an islaiuL Santa Gru/. occupied hy C, olUacea, We 

of rlivisioru with die species produced at (^ach sle[) expected U) find strong discrimination, manifest(Ml in 

differing according to llie particuhn- ecological the pattern of conlrasls shown in Figure 1 (ah()\e). 

circumstances that guided each patliway. This was Instead we found little e\ idence of (hscrimination of 

our starting point (I*. R. Grant, 1081, 1999). heterot\|)ic (hcterospecific) song on either ishuid 

Furthermore, we helieved most niclie space would (Fig. 1. helow). This is fascinating Ijecause it contrasts 

lie occupied in the early history of the radiation, with with clear discrimination between sympatric and 
later spet'ialion resulting in gap-filling, as ilhislral<Ml 

vouuiic^r species 

fr t—- -I- 


would have thought warhlei 


tly hy Jonathan Losos and colh-agnes wilh 

finches of the two grouj)s have surely liad enough time 
Caribbean Anolis Daudin lizards (I hu-nion el ah, to diverge in both beak morphology and song to enable 
2003; Losos et ah, 2006 this issue). Yiw experimental tl 


to coexist without interbreedins:. Yet the 

and observational work we concentrated on the ground im])licatiou of the playback results is that the oldest 

finch twigs of the phylogenetic tree, because these 

(allopatrie) lineages would interbreed, whereas tlit^ 

species are most similar to each other and have be<m \oungest (sympatric) ones do not, or do so \^vy rarely. 
genealogically separated (or a short time. To see if the 

a long lime (Petren et ah, 2005). 

Moreover, the genetic evick'nce tells us that despite 

same pnicesses of divergence in morphology and song their aj)[)arent potential to exchange genes, they have 

occurred early in die history of the radiation, we ha\e not done so, at least not lo an ap])reciable extent, for 
gone to the base of the tree. There, five years ago. we 

encountered a surprising fact. The initial divergence^ Theic are three other implicatioirs of this striking 

is frozen at the allopatrie stage. Reconstructions that c untrast (B. R. Grant i.^ P. R. Grant. 2002). The first is 

have used both mitochondrial and mudear genetic tliat rates of song and mor])hological divergence vary 

niaikers (Freeland & Boag, 1999a. b), including among the species; hence, the rate o( evolution of 

microsatellite DNA (Petren (^t ah, 1999), show a basal sexual isolation varies considerably and is not a simple 

split between two groups ot warbler firulu^s that are function of lime. The second is that either divergence 
no\\' allopatrie on different sets of islands (Petren et 
ah, 1999: l^.mil.s et ah. 2005). 

in song is accelerated in sympatry, perhaps hy 
seleclive reinfoicenicnt ol initial diflcrences if o(I- 

Why have they remained allopatrie? What has spring of mixed matings are at a selective dihadvan- 

[)revented them from eslablislnng sympatry? We do tage, or establishment of sympatry is made possible 

not have coni])lete answers lo these questions. Part ol onlv by the acquisition of [ironounci'd song differences 

any answer requires greater knowdedge than we have in allopatr). The third ituplication is that a knowdedge 

of ecological o[)portnuity for joint occupancy of an 
island. Anoth(M- part re(|uli(^s knowdedge of potential 
reproductive isolation, and this we do have. 

of neutral genetic diffej-ences among taxa in yc^ung 
radiations like Darwin's finches is not enough for 
inferring their potential to interbreed and ex(diange 

Morphologically the two groups of warble-r finches genes. Geographical, ecological, and behavioral in- 
are similar; corn spondingly, they are similar ecolog- formation is needed as well (Petren et ah, 2005; 
ieally as well. They also share the peculiar feature of Tonnis et ah, 2005). Ferguson (2002) has argued 
reversed sexual dimorphism in beak length, in wdiicdi similar points more generally. 
trait they difh;r from all other Darwin's lini h specdes 

and from all continental relatives (P. R. Grant & B. R. Spfxirs Rt:c()XSlDERED 
Grant, 200.*5). They dilTcr from each other to some 
extent in plumage color and beak si/e, but scarcely 


t tl 


enough to prcv(Mit ttiem trom niterl)ree{liug to juflge 




rom ( 

According to Graciaft (2002), the first great 
question of systematic biology is, what is a species? 
lifferences in pairs of sym])atric species of Templetou (1989) has suggested this question must be 
l)ai"win"s fincdies. However, their songs do differ (B. R. answ^ered before the process of species formation can 
Grant & P. R. Grant. 2002). With a focus on the be investigated. Like other evolutionary biologists 
([uestiou of the origin (tf reproductive isolation, w^e attempting to understand speciation, we have not 
performed a set of playback experiments similar to heeded this advice, histead of defining the species we 
earlier ones in which we simulated immigration of study, we have found it sulficdent to simply invoke the 
birds from another island (B. R. Grant & P. R. Grant, biological spe(des c:oncept with its einj)hasis on the 


Annals of the 

Missouri Botanical Garden 

Expected Response to Playback 



on o 

f ivprixluclive isolation and iiol 



classi float Ion (Harrison, 199!!; Hudson l^ ('on' lie, 

2002). Do Onoiroz (1998: 6:5) has followed iIk^ 
[»aI('onlol(>gisL C. C, Sniipsoii (1901) in arguinj^ "(here 
is rrall} only one gonfM'al spcoios ooru-('|)l ir] tiiodorn 
s) stomal ic and evoliillonary hiolo^;) — spooios are 
seginonis of population level e\()lnlionary lineages. 
lie then offers an iniportanl dislinetion: "A species 
coiiccj)! IS an idea ahoni llie kind of enlitx re[)resented 
l)v ihe si)eei(^s eatf^'ron. that is. about the kind of 

ihe term .syxv/ev. A species 


entity designated Ij) 

criterion is a standard h)r judging whedier a partienhu" 
taitily finalities as a member of the spi-eies category, 
thai is, forjudging whether a [)artieular (Mitity is or is 
not a s[)eeies" (de Oueiroz. 1998: 6.')). This neally 
bypasses the plethora of tangled arguments about 
speei(^s eonee|)ls and allows debate to be focused on 
how sp(Maes shoidd be reeogni/ed. 

ayr (1942) defined species as gron|)s of 

aclualK or potentially uiteiljreeding natural jtopula- 

lions, which are re]^rodueti\ el)' isolated from othfM' 

Observed Response to Playback sueli populallons. TIk- criteriouhere is ch^arly one of 

in tei breeding. A pp Meat ion of this definition to 
indi\ idnals in order lo refer them to speeie.s has 
repeatedly ejieounte red practical dillicnlt ies watli 
alloiialric pojtnlations and with poj)u]ations eonntH'led 
occasionally oi- rarely bv in Lerb reeding- (/ink & 
McKilrick. 199S; ^ce Aviso & VlOllenbcrg, 1997, 
and Wake, 2000 this i.^sue). These [)raetical diflKail- 




Lies have bet mi faced head-on b) 

systematists. For example, the Ta\on(tmie Sube(tm- 

niilteeofthe llrilish ()rnillioh)^isls" t'nion coub-onled 

them in draw ing up gui 


nes to assist in llie 

asses.suHMit of species rank (or the British Hii-d 
Species List. They stalled with a position slalement: 



we (leiuie species as po|)nlation lineages mam- 

* fl 



ir integrity with respect lo othei- such 

C. olivacea 

Santa Cruz 

Figiii-c I . Kxju'clrd (ah()\ e) and ohsciM d (hi-liiw) re- 
sponses (>( warbler limln'S on Santa (an/, [(Ivrlhiflra olirdced) 
and Ccnif\ ((L Jusc<i) to plaxback of songs i-ccorded on 
Santa (aaiz (?C), l-ai)cia (I). r,i'iin\csa (C). and Finta (P). 
Rcsjionscs iM^i' scaled to 1.0 on eacli i^land where 
experiments were eondiieled. (.^xili-ols wvvr (lassin's (null 
(CV) stHij^^s |-eeoi'de<l in \optli \nieriea. Populations on Santa 
Cru/ ajid Isaheki ln-JoMi: to llie C. olii <ic<'<t [ineai*e. and 

lineag<'s through time and space, this means that 
species are diagnosabi} diflcreni lotlicrwise we could 
not recogni/e iIkmii), reproductively isolated (olhta'- 
wise lliey wouhl not tnainiain [hc'w inlegritv upon 
contact) and members of each (sexual) species share 
C-. tllSCCl '^ eominon mate recognition and ferlib/at ion system 

(otiierwise the) would be utiable to reproduce)*' 

Genovesa (h^^h^'^ *^t ^>i-^ 2002: sio). 'Hien ihc) foil 

two reeomuK'ndallons. hirst, 'Mliagnosable taxa will be 
ranked as species if they are broadiv s\ tnjialiic. ia-'., 
over arenas beyond the average iialal di>|)ersal distance 
of the species iu\ oh cd.. . . and do not In bi'idize. ... or 
ln])ridi/e onl\ rarelv, so that ";ene fh^w between them 
either does not oeeui' (])eeaus(! liybrids are steille oi' 

owed w ilh 





populations on fienoxesa and Pinia heloiig lo the (.. fiiscn 
lineage. iM'gnre has(nl i}\] P. H. (;ianl S. P. \\. Cranl. 2002: 
(lii. 3 (©2002 \>^ die InixersilN of Chieai-iH. 

do not backcross for other reasons) oi' otMairs at 

a low frequency (oflcn difficult to delect) that it is 


LnnU\ci\ incu" giaie [)ools win e\'e!' merge. . . 




el ah, 2002: S22). Seeoiuh allopalric po[)n hit ions 

Volume 93, Number 1 

Grant & Grant 


sliouhl be considered dilleicnl species 'If lliey have useful In systematic studies of other groups of hirds 
diveri^ed to ihe extent that merging of their gene pools (Ahlslrom & lianfl, 2003). 

in die future is unlikely^^ (Ilelbig et al. 2002: 519), 
whereas, "pn^lictions al)out possible reproductive 

The s{H-ond prol^leni has no simple sohition. "We do 
not know of a single documented case of Ijreakdown ol 
isolation betwec^n allopatj-ic taxa that differ only reproductive isolation (i.e., a reversal to fuh re- 
sbghlly (e.g., in size or darkness of plumage) are very productive compatibility between st)ecies that were 
uncertain. Such taxa are b(^st treated as subspecies" incompatible l)efore) in any class of organism" (llclbig 
(Heibig et ah, 2002: 519). On the basis of the latter, ct ah, 2002: 521). However, Kal (1985) deserib(Ml 


recogrn/.ing our ignorance oi posl-matmg com- 


a possible case of breakdown of re[iroduclive isolation 
patibility, the warbler fluches are best treated as with two species of .'1;7<:>r/o/?/a L. freshwater mussels, 
subspecies. We consider them to be well-diltereuli- 

ated gen<^tic lineages. 

According to fossil evich^uce, they coexisted without 
interbreeding about 200,000 years ago, and now al the 

These ]n-escriptions for sympatric and allopalric same locality they hybriih'ze relatively commonly. The 

spec'ies fit \ery well with our past 30 years of two finch species on l)a[)hne may become the first 

thinking aud [practice based on the biologic:al species exception lo be witnessed in progress. At present di(^y 

concept and notwithstanding the fuzziuess (Harrison, are on a reversed course of speciation (P. R. Grant et 

1998; lley, 2001; Lee, 200:5) of specit^s boundaries a!., 20(H), in fact they are dcspecialing, and the point 

caused by rare hybridization. The prescriptions at which they should no longer be considered two 

clearly a])|)ly to sexuall) reproducing species genet- species, but only one, is arbitrary. IVIori)hological and 
ally and not just to birds. Nevertheless Dai win's finch 
studies ex])ose t^vo hidden problems with the lii- 

agnosis of sympatric species. First. s|)ccies may lose case lliey will be respcciating. Many other pairs of 

diagnosabilil) . Second, if ihey do it is an arbitrary 
matter to decide when they lose their species status. 
At the b(^ginning of our study on Da[)Ime Major 

Ceospiza fori is and G. scandens were diagnosabh' 

genetic convergence could easily be reversed if there 
is a change in climate and food com[iosilion, in which 

taxa, not Just Darwin's finches, might go [hrougli 
similar mcrge-and-(hv(M'ge oscdiations, as in some 
shifting hvbrid zones (e.g., Carney et al., 2000), 
possibi) also in young adaptive radiations such as the 

different on morphological criteria (P. R. Grant. silversword alliance in Hawaii (Barrier et ah, 2001; 
1993). With hybridization, backcrossing, and natural Raldwiiu diis volume) and cichlid fish in the African 
selecli(m occurring, the po[)ulations have converged Great Lakes (Salzburger et al, 2002; Smidi <.^^ 
in nu)ri>hology and are now^ more similar than tiiey Koriificld. 2002). 

Such fluidity can be bewildering to those who 
recognize s|)ecies by inferred ancestr) rather than by 
100% diagnosably different on the same morpholog- interbreeding and its consequences. For instance /ink 
ical criteria. Have \\wy lost their species status in (2002). basically restricting attcnlion to the lack of 

were at the begiiniing (P. R. GranI & B. R. Grant, 
2a; P. R. Grant el ah, 2004). They are no lougcr 

a couj)le of decades? They are merging, but very 

differenliation in mitoi'hondrial DN A among species 

slowly. Members of the two populations can still be- (Freeland c^" Roag, 1999a, ]>; Sato et al., 1999) thai art; 

uplicld by otlu^r criteria, lias argued ihcie are far fewer 

recognized by us on the basis of the song they sing 

(males) or the song of their mates (females), as well as species of Danvin's finches diau are currently 
by beak morphology in almost all instances. 'V\\v rccogniz(ML perhaps only half. Aside from an \\n- 
problem dial this poses for the delineation of species fortunate reliance on a single, potentially nnsleading, 

is that song is a learned, culturally inherited, trail, molecule (Ballard et al., : 


Nil son 

& C 


without a genetic basis in many species of birds, and 2002; Ferguson, 2002; Machado & Ih-y, 2003; Rokas 

yt^l "...characters used in diagnosis must be the et ah, 200;^). a view such as lliis overlooks the fact 

result of evolution: diey mu.-.! be geneticallv based and that as many as 10 species coexist on the same island. 
not merelv caused bv environmental factors such as 

ecologicallv differeiitlat(?d, mor])hologically recogniz 

nutrition" (Ihdbig et al„ 2002: 520). A way out of this able, and reproduclively isolated by song 



lilemma is to broaden the basis of diagnosis l)y morpliology (P. R. Grant, 1999) 


thai cultural inheritance may be as 

These [)roblems ilhisti'ate the well known fact that 

im[)ortant as genetic inheritance in trans-generational systematics deals with discrete caI(^gories, whereas 

maintenance of biologically imporlaul Ijaits used in evolutionary change is a continuous and gradual 

i-eproduction. We recommend this because song is the process (Harrison, 199o; Hey, 2001; lley et ah, 200:^). 

cullural eciuivalent of die Y chroimtsome in these Darwin's finclics are valuable to evolutionary biolo- 

birds; paternally i]di(M-il(Ml, non-recombining, and gists precisely because they so well exemplif) the 

subject to chajige only b\niutation, cullural mutation graded natu]-c of evolutionary transitions. Tl 


a re 

in this case. Song variation has been found to bi 

challenglug to syslemalisls for ihe sumk^ reason. 


Annals of the 

Missouri Botanical Garden 

Co\si:i;\ \T!()N 0! nH)i)i\ Kiisir^ 

BiiwiJinn. R. I. 19<).'^ TIk^ cvnlntioii of s 




] Dans ill's 

III uaiiviii s 

fiiu'lios. rp. 237-.^"^7 /// T\. I. Howntaii. M. Rcrsdti tK A. K. 
Ix'vitoii ((Mlilors), rallcriis of Livijliilion in (iaiapagos 
Organisms. Aincriran Vssoclalioii for' I lie AiKanii'inrnl 
of Scirnco, Pacific l)i\isioii, Saii Fiaiu-isru, Califoiiiia. 

ISiinis, K. J.. S. J. lla.-kctt .K N\ K. Klein. 2(){)2. ]Mivloi^cno[i( 
it'Ialionsliips and inoi'pliologjcal (li\ civih 
finclies a!i(l llioir i"<'lati\es. K\'(iliition ."^C): 1210—1252. 

Ca(l(\ T. j. I*)ii3. Ih hridizcilioii and jroiic cxchaiiiic anionu 
l>irds ill n-lalioii !o consoiA alioii. Pp. 2<io-^M)'J /// C M. 
Schoiu-waid-Cox. S. M. t^liaiiihrrs. B. i\Ia< liiMlc iK \\ . L. 


Thomas (cdilors), (iriu'tics and Coiisoi\ alioii. Rciijaiiiin/ 
(aiinmings. Monlo Park, California. 
Canun-. S. K.. K. A. {;ard!ior ..^ L. H. Riosol.oi-'!,. 2000. 



Ld J* 

volulionai'v changes ov(n' tlu 

Darw iiTs fiiKdu's arc \alual)le to (■onser\ alltm 
biologists for another reason. Tlicy deliver a n^essage 
aboiil preserving hiodiversiu ; since species, like llt<Mr 
environments, aie conlinuallv rdiaimint^. both nuisl he 
conseJAcd lo allow adaplalion [o fnitlier change. For 
any gi\en (oral species, or ev(t]nt itwiarily significant 
population of llie species (Hey el ah, 2003), other 
species in iIk^ coninuinily are pa!'l of ihe environment 
he they lood, comj>elilors, predators, or parasites. This 
is especiall) clear ni the case o( inleihreeding 
species, because their ecological and cvolulionary 
fnture di'pcnds to some exteni n|>on the genes th(^y 
e\(dKtnge with each other (Cade, l9o3; 15. H. CranI & 
P. R. Grant. 19i59: RliMuer & SimluM-loff. 1996). It is 

(dear with eonip(4itor sI)eci(^s that persist oidy ^^hrn ^^'■;'';'';'^^- .b^-'*''*-'- Tlic^ seven^ great qucstii.ns of sNMcinalir 

prtulators prevent one species fioni com|K-tiiig tlu^ 

others to extinction (Paine, 2002). It is (dear bom the 

depcndcnc'e of fiiudies (B. R. Crant & P. R. (bant. 

i9o9) and primates (T(M"borglu I Oo3j on one or two 

specific food sources at seas(jns of acute food 

limitation. And it is (dear from the mvriad indirect 

(Tfecls thai arc manilestcd in the trophic networks of 

co!nplex communities (e.g.. Wootlon. 199.'5; Davton, 

iilt\'-\('ar liistory of 
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Frederic Achate^ Timothy ./. Mofley,' Porter P. 
Lowry II,'''' and Joel Jerrmie^ 


The ^ciuis Citclliinla (Cufltiinlt^ar-iiuhiaccac) roi]]|>ris(^s aijpioxiiiuacly 150 spcries, rangiii- from ri\--\rvu Africa through 
the Inlands of tli<^ Indian and Pacific ()c<'ans to the Neotropics. Seciiiciice data from ihc inudear ribosoinal DNA internal 
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within (nuTtanh-ar. The results in(heate ihat Gucllcnld and l\\o smaller genera, /W?/;r/R'^i and Slcno.stomuni, are polypli)lctic. 
Most Ciirtfardd sjiecies fall into two disliucl giou[)>: a Xcjliopical Hnea^e that also includes the widespread Iiido-Pacific 
strand species G. speclo^a (the type of the genus), and a ^^'^^ Caledonian lineage that, along with AnU'rhra and Timonnis, 
cunipris(\s a (hoccions Paleotro[)ical cladc. The Hawaiian endemic Bohra. Iradilionally considered close lo Timonlus and 
assumed lo be of Old World origin. app«\u-s to be mor.' closely ndatcd to Neotropical GuciUirJa species, suggc>llng dial dioecy 
may ba\e (nolvf^l twice within the tribe. The use of tra(htional guioeciimi characters to delimit genera Nsilhin Guctlardeae is 
not' congruent with the ITS ph\logcny; other features, such as innorcscenc(^ architecture, sexual system, and palynology. 

a[)pear lo correhile more clostdy with the molecular phylogcny. 

Key north: bioge()grai)hy, dioecy, Curifanld, Ciu-ttardcac. islands, ITS. Neotrojiics, Paleotropics, Rnbiaccae, 


Rid)iaceae. one of tbe largest lanniies oi iioweriiig 

si k 

f n 

6 so 

plants with ca. 13,000 species and t):>u genera 
(Del[)n4e, 200 1), coin]nise 44 tribes (liohbreclit, 

1996: Kova, 1999; Kova et a!., 2002; Andersson & 

Anton(dh\ 2005). 

As })art of a systematic study of the New Caledonian 

1988) currentl) assigned to three sul)families (Bremer species of Guctiiivda, a niolecidar jdiNlogenelic 

& Jansen, 1991; 8retner et al, 1995; Bretner. 1997; analysis was condLieted to evaluate the monophyly of 

Bremer et a!., 1999). Tbe genus Gueltardu L. and its this widespread tropical genus, wliose definition has 
relati\('s have been retrarded ior most ol the last two 

\aried considerably . Originally deserilunl by hinnaeus 

centuries as 

a fairlv eh^ar-eul group, gcM^cM-ally (1/53) as monot>[>ic, GiwUarda has progressively 

giown with th(^ description of additional species and 

recognized as tril)e Guettardeae, and sometimes evc^i 

as a distinct subfamily under the invalid name the incdn^ion of at least fixe other genera: Malthiola L. 

Guetlaidoideai^ [= Antirhcoideael (Verdcourt, 1958; and Laup^ieria Jaeq. (Lamarck, 1792); Anlirhea 

Bremekamp, 1966). While assigruHl to subfamily ("/ln////7/om," Mu(dler, 1875); and, more recently, 

Antirheoideae by Robbnndu (1988), a series of recent 



molecular phylogenetie studies have shown that Roem. & Sehull. (.Staudley, 1931). The broadest 
(kiettardeae are best placed in Cintdionoideae definition of GncUarda by far was tlial of Baillon 
(Bremer AStrnue. 1992; Bremer et ah, 1995; Bremer, (1879, 1880), who inckubnl all Guettardeae species 




' \\r tliatik K. Vi'ur.lack and W Dcli.n-tc lor helpful advice; 1). bebR^au-Callen for lier Invahiabh' assistance and for advising 
the first author durin- his pollen study: iuo anornnions reviewer^ for providing uscliil coiiniicnt.- un an eadier version of the 
nianuscri])t; N. Dainico for l.clf. with pVr|.aring pollen samples; and T. JalTrc, G. Da-ostini, and F. Ri-ault lor their hosj)ilalily 
in New Caledonia an<l Un access to facilities al IK I) (Noumea). We thank the Dirrrfion des Ressourrcs Nalurellcs of the 
Proniuv Slid and the Sern'cc Forels, Bois el Enrironnemenl of the Prnrinre Nord in New Caledonia for |)ermIssion to collect 
speeimi'ns; the curators of CM, NOU, NY. and P for providin- access [u lli.-ir eoltccliuns andA.r for allowing the removal of 
material for molecular analysis; the curators of CAN b, L. MEL, and Z for loans of sj^ccinnMis; and C. Areci^s and K. Y. Tarn for 

leaf material [Preserved in silica gel. This research was conducted with hmding from the Progniinme 
Planforinaiions — Biodiversifr Tcrrestrc rn Nourellc-Galcdonie oi the ;l///,sc';//// National d'Hisknrc Nalurdk (Paris), a gilt left 
by II. S. MacKec, onf- of the most important speciahsls on the flora of New Caledonia, and tlir Lewis B. lS: Dorothy Cullman 

Foundation for molecular studi(\s. 

niie (Mhtors of the Aiuiah thank Sophia IJalcomb for her (Mlitorial conjribulion to this article. 

■'Museum National d'lli^loire Nalurelle, DepartfMm^it Systcmatiqne et Kvolntiori. bSM 602. .S7. rue Cuvier, CP 39, 

Paris CEDEX Oo, France. achille@mrdindr. 

^The Lewis IL and Dorodiy Cullman Program for Molecular Syslemalics Studies, The New York Botatiical Carden, Bronx, 

New York 10158-5126, U.S.A. tmotlcyCq' 

^Missouri Botanical Garden, P.O. box 299, St. Louis, Missmiri 63166-0299, U.S.A. pete, 

7523 1 

Ann. Missouri Bot. Gaud. 9:5: 103^121. PiBLisiibu on 31 May 2006. 


Annals of the 

Missouri Botanical Garden 

known al the time. Schuttiann (1891) rejected on lliese markers ])laee the six Ci/rlUirdd species they 
Raillon's ideas and ?-eslricted the circumscription of sampK'd in a polylomy alon^ uith several nlVwil 

genera, viz. (Jionirlid. Mahirica. Neolaugcria. Slenns- 

Gucitanld, excluiHng laxa usiiail) |)laeed in Aulirlied 
and Ldn^ierid. \\ Ink- ScluuTiann's concept has I)c(mi 
followed hy most anihoi-s since (e.g., Standley, 19:51; 

fomitn} (referred to as Anlirlwd), and Tinioiiius. 
(>onsi<lciing die \vid<' ram^e of inler|)rctat ions (oftt^i 

^ - I- ^ 

Bremekamp. 1966: Airv Shaw. J9.;3; Sleyermark. contradictory) of relationships hased on tlie morpho- 
19^2, 19cl; RohhrecliL I9<SP)), a mo(ha-n comprchen- h)gicaK hiogcographlcal, and molecular data, il seems 

siv(^ review of the gemr^ is lacking. 

opporlime to examine more closeh the nhvloireneli( 

Cuelldidd is currenlly regarded as a largv, nearly slatns of Cucdanld, as currently defined, and its 

affinities \\l[\\ \l^ apparent close adies. 

Gucftarda and the othei- genera currenlly included 

c generally grou])c( 

pan-troi)ical genus of trees and slnuhs. It is 

charaeleri/(Hl by flowers with usually imhricate 

corolla h)hes. 2- to 9(lo 2())docular hiiits with a stony in Cnctlardeae (Tahle 1) ar 

endocarp and one seed per h)cnle, and a non- logetluM' l)as(Ml on a set of common characters 

persistent calyx, hi the N(M)tropics, Cucltdnla is including: a woody habit, entire hilcrpellolar stipules 

dionght to comprise an\ where from nearly HO (Taylor (divided in Neohlaked), axillary innorcscences {Wr~ 

el ah, 2001) to more than i;50 species (Andersson, niinal in Dirliihnilhc, Mdchaonia. and NeohUik 


1992), and is morphologically ([uilc hetciogencoLrs, 
including laxa originally described or placed in 
several geufM-a once regarded as distinct, 

a single, apically atlached. pendulous 


s o\uie ni e 


cell ol the ovar\, (leshv fruits with 2 

to many 

(' (r 

ujiilocular [>\ renes or a phnilocnlar cudocai-p or 
pulameii (dry capsidar fin its in Machdonia), and 

Dicrobofrytini, Ldiigiciid, MdUluold. and Tounicjor- 

liopsis. Fiulhermore, the inclusion of Andrhca (or (>longaIcd sct^ls ullh |>ooil\ -<lev<doi)cd 

Sfniosloinmu, lo which Neotropical Anlirhra species (Rohhrcchu 

are lanivutb assigned) can also be inferi'ed hased on 


1988). Using this definilion, tlii' tril 


contanis perhaps 12 to 13 genera and moi(^ than 


the reeenl placement of the South American species species, ranging in distribution from coastal East 
A, siirinafdcnsls (descrihed b\ Rrcmekamj). 1959) in 

synonymy under GuelUnda dcrcdna K. Kn 
Taylor el ah (200 I), 

In tln' raleolropics, a single, coiiimon, 





Africa to l^)l) nesia and the Nfn)troj)ics (Aclhlle, 
unpuhlished (hita). The Mtiabsis of Rova el ah 
(2002) using se(picnce data h'om the chloioplast //v/h 
inlron and /n/h-F spacer suggested a nmch broader 

Pol V nesia, accounts for most 

sptM'ies [Giictldnld spcciosd h.), whicli ranges h-om eircumscription of (hu-tlardeae (Table T) ihal inchidcr 

several genera formerly placed in two other Irilx^s, 
Iseiliac and liondeletiac. However, the expanded 
notion of (h]cltar<l<'ae pro[)os(Ml |}y Rn\ a el al. 
(2002) s(H'ms |>rohle[natic hei-ause lh(^ additional 

le o ler 


eastern Alrica to 

o( Gurildrdd'9' broad distribution. 

World species (ca. 25 in all) are ahnosl 

sively nai'row endemics on NeAV Caledonia an(. 




com[)ris(^ a mori)hol()gicall 

\ tlncrse 


r n 

lese taxa ihev included h; 

ive morftiiologK^s 



were assigned lo GiwUdrda by Jhiillon (I879j and different from lliose of Cu(4tardeae s. str.. as refleeled 
Cuilhunnin {V)\[\) in accordance with llieu' broad b\ the fad thai elemenls (whose distlncljve 

features include slricth' terminal iriflorescenc(\s, 
mostl) pluriovniale locules and capsular fruils. or 

concept ol iIk^ genus, allhongh they difha" from its 
other members by several important characters In- 
cluding a dioecious sexual system and a persist(Mil 
calyx. As currenllx cirtannscribed. ihe genus Giicl- 

fdnla thus has two main cenka's of diversity, the deae, wheivas Cucttardea* 
Neolropics and New (Caledonia, showing an unusual rheoideae. 

sometimes sub-caj>sular fruils in Godzaldgiuiid) were 
])laced by Rol)l)recht (1988) in subfamilv Cinchonol- 

were assigiK^l to Anli- 

Irans-Pacidc distribut i(»!i shart^d with onb a lew olhei 
genera of linbiaccae, such as Au'rusia 

Roll! sensu 

Kirkbride (1997) (including Lindcfji'd Benlh.) (Roh- GurUanld 

W ithui Cucltaidcae (sen^u lutl)l)rec:lil), several 
elements appear l(t be most closely relaled to 

brcchl, 1988). 

(as curr(a]tl) circnnrscribed). logt^her 
comprising core Cucllardcae (as defined in H^abh' 1): 

R(H'ent moletadar ph\logenelic studies have pro- v i/- -4////W/c^/ (in(-lu(ling rw/cZ/f/zv/cZ/r/), /^/vca, r://o//;c- 

VKied lilt hi evidence rcHianhnii the mononhviv (tf 


CjicNanld. Molecular se(iuence data htr the genus are 
scaixte, iwul. apari b-om ihe inclusion of a hwv species 
in (amily-level phylogenies, ihe onlv taxa studied lo 
dale are those used b) Rova (1999) and Rova el al. 

' monophyly of //(/, Guclldrdd. Mdlanca, Nvoldutivna, Ouoschniidlui, 

Pfli(}iiii)i!s. Slcdoslomum. and Tiinonius. These 10 

genera (orm a morphologlcall) homogtaicous group 
whose recognition \^ consistent uilli avallahle molec- 
ular dala. In ihe ph)logeni(^s b-om Rova (1999) and 
(2002), who (^xamined rps^(^ and //v/h-K se(nien<es of Rova ct ah (2002). the core Cnctlardeae ihev sampled 
a Imiiled number of e\emi)lar laxa. Mowever, due lo (except nohcd) comi)rise a slronglv sn])porled mono- 

insudicient levels of s(niuenee variation, trees based 

phvletic grou]}, while the remaincha- of the Iribc (sensu 

Volume 93, Number 1 

Achille et al. 
Polyphyly in Guettarda 


Tahic, 1. Genera included m Gucttardeae by Uohbreclil (1.988) -dud in llie "Guellardeae" sd. cladc in tlie pliylogenirs of 
lJ(.va (1999) and/or Rova et al. (2002); lliose ivtainrd ni nnr (Hiettardeae (as defined here) are indicated in die ri-lil colunni. 


excluded: n.s. = genus not studied. 


Allcnanlluis StanfU. 

Anlirlicd Coinm. ex juss.' 

Anichnolhryx Planch. 

Bohea Gaudich. 

Clioificlia Jaeq. 
Ciiairccasasiodcndron SUuidl. iK 

Dichdanihe Thwaites 
Conzdlas^unia Ruiz & Pav. 
(.iK'ilitrdd T^. 

(riicllanlclla Chanip. ex R(Mitl 
JdiorLiJCd l^orhidi & Konilodi 
Miichdonif/ BonpL 
MaUinea AuliL 
Svobldl'Cd Standi. 
Neuldugcria Nicolson 

OlfoscJmildUd L'rb. 
Rof^irrci Platich. 
pLilonlolis Griseh. 
Stenoslonmm C. F. (kieiin. 
TiniDfiius DC. 


Gu(4tardcae sensu 
RobhnM-ht (P)c'i8j 

























within Aniirhfif 


Guettardeae cladc of Rova Genera in ci>re Gucttardeae 

(1999) iK Vunn el al. (2002) 
























J iniodiiis 

' Sensu Chaw & Darwin (1992), 

'" Genera assigned to the core Gucttardeae clade by iuua (\^)99) and/or i\o\a 
•^ The authors actually sam]^l(Ml only one species, \nfirli<-(i dculdld (DC) Urb.. ulnc 
(Borhidi cK Fernandez, 199:^-1991;. 

(^t al. (2002). 

(a.-, dcniicil here) 



Bohr a 

within Anfirhea 







h is currently placed in Stcnoslomiim 

Hohbretdil, 1988), exeeiit DichUanthe (whifdi was not lion, we liave tlius provision 
satnpl(^(l). are scallercd atnoiig a paraphylelic group. 

ally eliosen to regani 

Furthermore, core Cuetlarileae, as circuniricribtid 

Bohea as a UKMnber of core Guettardeae. 

Circuuiscriplions of the genera comprising core 


lere, w 

du(di correspond to BaiRon's (1879, 1880) GueUardeae lias e varied widely from one treatment to 

broadly defined GurlKirda, display none of Uie another. T 


fienia'a, AuUrhea and Tinionius, m 

distinctive features (menliotuMl al)ove) that chLn-acler- addition to Gucllarda itself, play a central role m 

i/.e Dirhilanthe, Neoldakea. Mfirhaoida, or the genera the group, as inosi species have at one lime or another 

newly inchided in the tril)(^ by Rova (1999) and Rova been associated with at least one of them. The 

et al. (2002). Neotropical genus ChorneUa (inchiding -4/ C. 

Althotigh Bohca lias always been iniduded m 

Presl) comi)rises ca. 50 species and may be associated 
(kiettarde'ae, Rova (1999) suggests that it wouhl have with GucUarda (Tayb)r et al.. 2004), as tbe^two are 
to be excUided in oider to render th(; circumscriiition 

difficult to (hslinguish from one another on the basis 

of die Ij-ibc (sd.) monophylclic. Morphology, however, of unequivocal cliaracters. For example, Schumai^n 

i>nivi(h^s very strong su])port for die inclusion o( Bohca 

(1891), Standh-y (1934), and Steyermark (1974) 

within the core group of Cueltardeae. B(dwa is hardly separated Chomclia from Gucltarda on llu^ basis of 
(Hstingnishable froM> Timonius, where il was placed in corolla aestivation (valvate vs. iml)ricate. respeclive- 

by CandoMe (1830), and Baillon (1880) ly), but Bnrgca- and Taylor (1993) recognized both 

aestivation tvpes in ChorneUa. Furthermore, IrnL-F 

s)'non) my in 

iiududed both genera within GucUarda sd. More 

_________ — _ -| 

recently. Danvin and Cluns (1990) regarJeJ Bubea as sequence data, althougli limited, suggest tliat the two 

dislincl,l)ut closely rclalcd Io77monn/.s on llic!)asis of genera are related (Rova et al, 2002), as the only 

morphology. In the fndd, individuals of Buhea are Chomelia sampled (C. tenidfolia Benlh.) clusters with 

Innnediateiy recogni/ahh' as belonging to Cueltardeae one of llie live Gucltarda species (6'. rrispijlora Vahl). 
on the basis of fruit structure and overall morpholog) 

Antirhea (including Gueltardella), l\culau 


(pers. ohs.). NotwillistantHng Rova's (f999) suggcs- Stenostomiwu and Pitlomolis appear to comprise 


Annals of the 

Missouri Botanical Garden 

a r{)nij)l('\ (.li,slril>utt'(l In llic XeoLiopics and the Iiulo- 

Pacilic n'i^ion, cliaracUM-izefl 

vaUalr corolla lohes and sppaiale pvrciK^s. Bobcd 

inil)ri(*at(' corolla lol)(\s, 2 [o 12 uiiiicd |)vrcne.s, and 

>> ttiostly 4 to S coiiiprisos four species endemic lo Hawaii (IJc 

i V\\ I ! I c 


(^liaw. 1090), vvliieh diffej' mostly from Tituonins by 

a persislenl calyx. All \\\v raleotro))ical species in ihis il,e presence of iml.)riealc corolla lobes. 

^ronp a])pear to be dioecious, a fael that was not 
discovei-(Ml milil rec'cnll) (Cliau & Darwin. 1992). The 
mon()l)|)i(\ Neotro])ica] gemis PiUoniofis^ deseriljcd 

Finally. t\v(» Neotropical genera, Odosrhiuidiia and 
Mahincit. staiid out because ihcii- eircuiuseriptions 
have rarely bt'cn (jucstioned. Ouoschmidfla (3 spe- 
by Crisebach (1858), is readily dislin-uished b) lis cies) is easily sf^paraled from other Cuettardeae by its 
lou-exserlcMl stamens, perfecl Houta-s, and panienlale 2-loeubir ovary and zy-omorphlc corollas. Malanea^ 

with ea. 35 s|)ecies (Taylor (M ab. 2(){)1), is recogiii/cd 


inflor(^sctaices. However, llemsley (1881) [rausferred 
PiUonioli.s to Anlirhea, a decision diat has 1 
lollowed b\ some authors (Schumaufi, 1891; l)\vy(a*, 
198)0). 1 hooker (1873) nuM-ged Slcnosloiniu/i, a Cai'ib- 
bean ^(uius, and Cuellanlclla, a small South Asian 
geuus. Into Anfirhra. Most subsequenl authors ha\e 
regaidcd Slcausloniuiii and Anlirhca as con^^enian' 
(e.g.. Sehumamu 189]; Staiidhn", 1931; Hremekamp, 
1966; Air) Shaw, 1973; Su-yrnTunk. 197 1; liobbrechl. 

by its 

twining habit, 

pam(ailate to splciform in- 


florescence, exserled stamens, and stijjules \ 
a dtstincti\(' morj)hology, all hough Tax lor el al. 
(2001) regard the distinction between Mdhmni atid 
Chomelia as un(dear. 

bi an effort lo evaluate dn' phvlogenctic status of 
Curftanid, as eurrenlly defined, we ha\e endeavored 

^^^^ . tt> include a re|)resentati\(' gron[) of speci(^s Ixdongitig 

198t)), Aceoi'dlng" to llus broad trenerie circumserin- i ii r ^^ ,. i ^^ i i 

^ , ^ . ' "i lo Ine geu(M-a of core Cuettardeae. Our study emplovs 

tioi], Anlirhcd, like CueUdrdd, e\hil>its an unusual 
trans-l*aci[ic disti'ibution. 

I^ecenlly, Janseti (198)1) restricted Anlirlicd to two 
sijccles n-om the Mascarcne Islands and Madagascar, 

and assigned all the olhcr Old W orld speeies lo 
(hicUdrdclld. His generic delimltalions were leased 
largely on die mnnber of flowers \v^r itifloreseenee, 
number of ovary ctdls, geographic dislril)ulion. and 
also an erroneous interprelalion of floral sexual i I v. 
By eonlrast. Chaw and Darwin (1992) retained all the 
Old World speeies in Adiirhea (36 speci(^s). within 
which th(;y distinguished tlnce subgenf^-a, .1. sub<'. 

Aniirhcd, A. sul)g. CdcKdrdclId (Champ, ex Benth.) 

Chaw, and A. su])g. Mesoiarpa Chaw, while lentatlvely 
suggesting that Slcdosfoniind repres(Mits a distinct 

DNA se(|ueiices from the Internal IranseribtMl spacej- 
region (ITS, si)acer 1 cK- 2, and 5.8S gene bdweeu the 
nuclear rlbosonial DiNA JHS-26S genes). Using 
a bioad sampling of 21 s[U'eies of Cdcl/drda (as 
current]) eiremirseribed) and 21 speeies belonging to 
10 other genei'a of Cuellai-deae (sensu Box a. 1999), 
w(^ thus (I) evaluate the nionopliyly of GucUdrdd: (2) 
|no\ ide some insights regarding the j)hylogenetie 
status of olIuM- core gencj-a In r(dation lo Guelldrda, 
especially those whose eircumserlptions 

]a\e \' 



y; and (3) attemj)l to idetitif)' morjihological 

characters ihal 


ight prove valuabh; for hu-|her 

s charac-terized l}y hermaphroditic, (4 to)S- 
nierous flowers, ebracteolate infl 




a N(M)li*o[>lcal distribution. Following lluar suggestion, 
Bt>rhldi and Fej-nandt;/ (1993-1991) formallv tians- 
ferred die 39 Aniialcan species of Adlirlica to 
Slenuslijnnun, and I'educed Neolddgcrid (4 to 6 
Caribbean species, distini^uished bv the united 

taxonomic and jihylogenetic studies wilhiii Cuettar- 
deae. We ha\<! also examined the geographic 
distributions of duefldrdd and Aniirhcd in light of 
iIh^ results of our phylogenedc analysis, a.^ ihese two 
genera ar(^ among the onl) Bnbiaceae to exhibit 
a disjunct, nt^arly pantropical tlistribulioii. 

iMatkki\ls.\mj Mktuous 

stipules afid the 4- to 6-locular ovar)) to a section of 

'lAXON S\\1I'1.1X(; 

Stcnoslomuin. However, Moynihan and Watson (2001) 


o ensure the best possibh^ repres(Mitation of 

rejecte<l the Incduslon of AVY)/r/?/g-e/7f/ \n Slenosloinuin infragenerie groups within CucUdrdd, foi- wliich no 

leased on pliylogenetic e\ldem:e fjoni ITS secjuence conij)rehensI\e infragenerie trealment is a\ ailabl<\ we 

\arlatiou of lliree species of \eol(/itgrrid and one of delimited informal niojpliological grou|>s on the basis 

The large genus T'uuonius is tradlll(tfi:dl\ r-harac- 

teri/ed hv lun i 



with separate pyrenes, 
alllu)Ugh this featuj-e is also encount«M-ed in Bohed. 

of examination of herbarium mal<M-ial at P and NY, 
field observations made bv the first author in New 
Caledonia, and liifor-mation gathered frotn die litera- 
ture (in iKutieidar Howard, 1989; Standlc), 1934; 

Timodids comprises uuuc than 180 s])ecies (Darwin, Standley & Wifllanrs, 1973). FurtI 
1991) disti-ibuled from tlu^ Seychelles lo Polvnesia 
and from the Plulipj)in(vs lo northern Ausiralia. It is 
mori)h(>logieally het(M-og(Mi(M)us, but is classically 
iiUer[)rc4(Ml to include all dioecious Cuetlardeae with 

uriuermore. we 

attempted lo imdude speeies bom various ]>l]ytogeo- 
;ra[)hieal subdlxlsions of the N(H)tropIcal regi(nis, as 

delined b) y\ndersson (1992). We have also sought to 
sam])lc. as exhaustivel} as j^ossible, al llie gtaieric 

Volume 93, Number 1 

Achille et al. 
Polyphyly in Guettarda 


(and sonieliiiu's infragencric) level within the olher hoard for lU) niiii, at roota temperalure, and llien 
core genera oC Gueltardeae. To delinnl infragencric ceutriluged al 14,000 rpni for 1 niin., and -350 [.[\ of 

consnlted ihe Irealments of Anlirhea l)y snpernalant was removed and added lo new Uihes 

lOSO |ll of Nal solution, 20 ).ll Glassinilk, 


groups, we 

Chaw and Darwin (1992) and Slcnosloniunt 1j) Hodiidi 

and Fernandez (1993-1994), and the partial revisions and 1 jll TBK modifier (Qbiogene). 'I^he tubes were 

of rmiu/;/u.s h) Darwin (1993, 1994), supplemented by placed on a tipping board for 30 miii. at room 

informal morphological groups that were identified in lemperalure. Afterward, the tubes were ceutriluged 

the same manner as Guclinrda (Valeton, 1909; Wong. at 14,000 ri)m for 1 min. atul all of the supernatant 

1 988) . 

was t 

liscarded. Next, each Classmilk pellet was 

Special attention was given to including the type washed three limes with 800 ^1 and once with 
species of each genus, and, wlien possible, a mininuim 150 |ll of ice cold New Wash solulion (Qbiogene). 
of 2 species were sequenced per genus, subgenus, or After the final vvasli, all of the New Wash was 
informal grouj^ The 42 taxa used in the analysis aspirated from the Classmilk pellet and 50 |il of 
represent 9 of the 10 core genera of Cucltardeae 10 niM Tris-Cl (pll 8.5) elution buffc-r were added lo 
(Table 2). Including the type species of o currently 
recognized genera {Giirinirda speciosa, Anhrhea 
horhoiiica. Bobca elatlor. ChomeUa spinosa, \rnl(m- at 14,000 rpm. The supernatant cotitaining the DNA 
^crid rcsiiiosd. Piltoniolis Inchamluu Slcnoslomum was removed and transfcrrtul to new tubes and stored 
luciduin. and Timoniiis limou) and 3 genera currently 
j)laced in syn(niymy, namely, Dicwhulryuni. (hiellar- 
della, and .Vlalthiola (typifi(Ml by Giteddrda diidrinild. 

resuspend (he DNA. fhe tubes were incubated at 
— 55"C for —10 min. and then ceiitrifuged for 1 min. 

at -20C. 

\}\\ A,\ 

je mcUn 

For DNA amplification, PCR was performed in 
hided, and a single species each was a 25 pi mixture consisting of 2.5 ^tl lOX buffer with 

MgCl^ (Perkin EIukm-, Foster City, CA), 9.3 |jl 

\j}tirhe(i cinncnsis, and Gueilarda sc(d)ni. respe(*li\('- 
Iv). Because of a lack of tnatcrial, Olfoschmidfia could 

not 1 

se(|ucnccd for Ghomelia and M(dauc<i. For Anlirhra 
luul TuuDfuus. we in(4uded 4 and 5 species, re- 
spectively. \\hich were selected to represent as much 
morphological diversity as possible. Three previously 
published setjnences were used for Neolaugcn'd 

autoclaved nanopure water. 2,.^ \x\ BSA (bovine serum 
albumin), 2.5 ^1 dNTP, 1 |.tl each of iwo 20 LlM 
primers. 5 |_ll bctaine. 0.2 |il Taq polymerase (Qiagen, 
Valencia, CA), and I )jl of genomic DNA. All PCR 
driisiflora. Slcnoslomum myrtijoiium, and Twumius and cvcle sequencing reactions were run on a C(Mie 
rnlidus (Movnihan & Wal.on, 2001). while 39 new Amp PCI! system 9600 (Applied Bios>stems, Foster 
Guettardeae' scf[uences were generated. Two outgnnip City. CA). The ITS region was amplified using primers 
taxa iCualrerasasiodendrnn speclabde and Gonzalagu- NY183 (5'-CCTTA'rCA^FrAAGACCA ACGAC-3') 

and NY43 (5'-TArGCT1^AAAY^rCACCCGGT-3' 

and when necessary hvo additional inlta-nal primers 




selected from Cuctlardeae sensu 

Ro\a. since diey are both placed near to iht^ genera ol 
core Gueltardeae in his |)hylogenies (Ro\a. 1999). 

Ave re 

emplo)cd, irS2 (5'-GCTACGTTCTTCATC- 

I)X\ r.vrHACTioN 

TAGC-3') (While et ah, 1990; Baldwin, 1992; Baum 

et al., 1998). The PCR conditions for amplification of 

Leaf sam[>les were collected either in silica gel or the ITS region were: 1 cycle of 9 / C for 50 sec.; 30 

fjom herbarium sheets. Genomic DNA was extracted cycles of 97"C for 50 sec, 53 C for 50 sec; and 1 

from approximately 1 cnr' of dried leaf tissue using cycle of 72"C for 1 min. 50 sec, hold 72"C for 7 min., 

a modified CTAB methodology. Leaf material was 
ground in a lysing matrix '\V' tube (Qbiogene, 
Carlsbad, CAj and pulverized for 15 sec in a Fastprep 
machine Fl^-i20 (Qbiogene) bead mill at speed 5. 
Subsequently. 500 |il of Carlson Lysis Buffer (2 g 

CTAB, 8.18'g NaCl, 0.745 g KDTA, 10 ml 1 M Tris/ 

llCl pH 7.0, nanopure water to 100 ml, verified to 
pH 9.5. autoclaved. then 1 i^ PEG 4000 added when 

hold at 4"C. 

cool) and 75 |J.I of p-mcrcai>loethanol were added to 
each tube and incubated at 74 C wilh occasional 
shaking for 60-90 min. Following incubation, 575 \\\ 
of SEVAG (24 : 1 chloroform : I^oamyl alcohol) were purified wilh spin colmnns from the QIAquick PCH 

D\A SEgLK.\(.].\f; 

To detect successfully amplified pi'oducts, as well 
as the ].)ossiblc |)resence of multiple ITS paralogues of 
varvin*'- len^ith (as discussed bv AKarc/ & W'etulcl. 
2003) and possible contamination of negative con- 
tnds, PCR pioducts were examined on 1% agarose 
gels stained wilh ethidium bromide and visualized 
under ultra\ lolet light. Amplified pnjducls were 

added to each lube; the lubes were placed on a tipping purificali 



following protocols pr()vid<Hl 


Annals of the 

Missouri Botanical Garden 

Tal)lf 2. S|K'cirs, ori-iii. and voucher inforniat ion for iIk- 1-2 ITS scqiu-iu-cs um-.I in llic pivsciU .MikK. \ou(lu-r 
iiifoniialion, wild collrclinns Italici/ctl. is givrn fnv urw s('qiK'iir(Ns; liu-raliitv cllalioji is proxidcd for |itv\i.)usly piihlisluul 
s(M[i]rric('s of llin'(^ ta\a. 1 Irrhariiiin a(a-()it3ins lollou Iiulcx llerhnnoniiu (liolniiirni el al.. 199()l. I^nti; 

indicated in p^nvndiescs follciwint; Ct'iiBanL accession nutiilirr. 

I s<'(]inM!C(\s ar<' 


Anlirhra horhonicd J. V. iUuc]. 
Aniirhra cliinrnsis (Clianij). vx Rcnlli.) 

V\ ]]. FotIh-s X He insl. 
Andrlu'd rhanuundvs (Oaill.) Cliaw 

Aafirlicd si/iilhii ( l-'o^lxa-*; 

Mcrr. t.K' 


. I' 


Bohea vUiiior (iaiidich. 
Bohra s(in(hri(i'nsls {\. (w;n-) Hi 
Chofncliif sj)in(».<i jact|. 


Giu'!!(ir(I(t (urvdiui K. Kran^t' 
Cuvllardii coinl/sn L i"lt. 
Ciicllardd irispifJurd \'alil 

Gucllnnld iUidvicdUi (Hiiinl). t.K IJonpl.) 

(riu'lldidd cUiplicd Svv. 
(jUCltdrdd hclerosrpdld (inillauiiilii 
Cfd'Uardd liirsiUd (Hiii/ X I'av.) I'crs. 
Ciif'lldrdd hunil}i}ldlcfisis (wiiilauiiiin 
(Uirthirdd hnii^ii Vvh. 

(hicffdrdd lUdcrdspvrnid Dunn. ?ni. 
(kietldritd iidinidCdVjxi Ufli. t^ I'^kinan 

CiU'itdt'dd mnuncdiid lialll. 

(Juctldidd noldmna Miiil. Vfi-. 
(lUelldrdd pim^cns L rh. 
CjjtelUudd scdi/rd (i..) I, am. 
(liK'Udnhi sp. "(aiha"' 
(du'iiardd spccinsd ! ,. 
Guettdidd sph'ndcns Hail 
Gui'!!dr<ld stinu>p}})llii I i 

(hiclUddd Irliiu'rd Ciiillaninin 
('Ui'UtU'dd uriKjdCfi.sis Cliani. iX Sclilldl. 




iNcw Calrdiinia 




('osla Kica 

Cudlrccdsdsiddefidrdn spcrlnhilc Slr>)'rin. Col 

(Idfizdldixiinid rosea SlaiuJI. 


Cosla Iiica 
Frcncli Oniana 







I'nfiln Kico 
New Caledonia 



New (.Caledonia 

PlHTio lu( 


Cioia Kica 

WVst Indies 

N<'\\ (^aledttnia 
I^ili\ in 

l*iimlo Kico 

Pnei-|(> Hieo 


^('W Caledonia 

New Caledonia 
Y\ esl Indies 

New Caledonia 


Mdlddcd nuwrdplnUd Hull, ex (wisel). Cnuma 

Ncdldiii^rrid di'!isijli>rd ((icisefi.) Nieoison 



Neolditiivriu rcslnosa (Vald) Nieolson 
PUidfiiolis /nchf/nfhd (irisel). 
Sfeiiosfdfiiiini dculdimu DC. 

I'licrio Hien 




Pnei'lo Kiel) 

Vonehei mformnlion / 

lite[-aliirT citation 

R(dd>ldindlazd 12 18 {V" 

K. \\ Tdfu s.n,. Iloni^ Konir (P 


[chilli' 6H8 ( 

A. C. Snnlh 7hHS (NY) 

Mdiln 2536 (NY) 

TdLrucIti 3302 (NY) 

ScifrIrr 12306 (KY) 

Kurd a <d. 2063 ((;n) 
Achdie sai.. Cidt. NYBC (P) 
Mdii 13HV2 (NY) 
Lnuz i't <d. 2353 (NY) 

Andrrssdft rl dl. 20111) {i'Al) 

Jafisrn 4903 (NY) 

A.xcl rod 3060 {m 
Arldllc 697 (P) 
Dclpii'iv 6034 (NY) 
Achillc 672 (P) 

Strunv 1 102 (NY) 
lldiunirl J 6333 (NY) 

IJdgicr 10631 (N\) 
At'hdir 662 (P 
Nee 10336 (NV) 
Gr lines 3261 (NY) 

Aceivdd Rodriiiuez 2310 (NY; 
Are<es 0333 (N^ 

/lr/;/7/c 661 (Pj 
/lr///7/e lOlO (P) 

LioLiier 16930 (NY) 

Aclulle 370 (P) 

HlCS 12227 (N^) 

JdNsen-Jdrnhs 3366 (NY) 
MoMnlian cK W al>on (200 J 

Tayldi <K: Gereaii 10304 {H\ 

Grodi 63 1 J (NY) 
Axe! rod 3283 (NY) 

Sienosfoiniiiu liiei<linn (Su . ) C. F. Gaerin. Dominican lvi-|)Ld»lic Aceredo Rodni^uez 3468 (NY) 

Slenosloninni nnrlijoliiun C.risel). 



iVloMiIhan iS W'atxtn |200l) 

Tiinn/fnis deiisiflorus \'ali'lon 
Timonins Jldicsecns Hakei' 
Thnoiuus ditidus I''ern.-\ il 

Papna NI(^w Guinea Tdleuehi 8639 (NY) 

hnddd e! <d. 13 (NY) 




Mownlian tX W alson (2001) 

Tiniodlus polygdunts (FihsI. f.l Piohinson Fiencli Pt>I\ncsia 

Mofley 2044 iNY) 

'finto/dus llnion (Spicng.) Mcrr. 

Pa[Hia New Guinea Motley 2309 (N\) 

GoiiPank acc-es.sion 






















Dy 06:5602 










Volume 93, Number 1 

Achille et al. 

Polyphyly in Guettarda 


1)\- the nuiiiuraclLirer. Purifii'd products were cycle beck & Ronqui^U 2001) using the CTK+l+f model ol 
sequenced witli dye terminator ARl l^rism® licady 

nueleolide substilulitm. a general time reversilih- 

reaction mi\ (Applied Biosystems) using dRhodainlue model thai allows (I) a proportion ol in\anable sites 
or Big Dye \ 1 .0 (1/8 reaelion) and 5% (hmelhyl 



(2) among-sIt(! rale lieterogeneUy loiiowuig 


a ganuna distribution. This model was selected as 

and hold at I C Proilucis were purified using 

sulfoxide. Primers for cycle se(iu(^nclng were the same 

as those used in the PCRs. Cycle se([uencing the l)est fit model for our data from a comparison of 

conihtions were: 1 cycle of 95 C for 1 min.; IV2 cycles 2 1 models using the Akaike iuformalion criterion 

of 96'C for 10 see., 50"C for 5 sec. 60 C for 3 min.; (Akaike. 1974) as implemented in MrAlodeltest 2.2 

(Nylander. 2004). a mochfied version of Modeltest 3.6 
h)drated Sephadex G-50 DNA Grade F colunms (Posada & Crandall, 1998). The analysis of the ITS 
(Amersham Pharmacia Bioteelu Piscataway. NJ) and data set (excluding iudels) was run usiug 2 X lO'* 
dehydrated in a s[)eed vac. The DNA was resusp(Mu!ed gen(M-ations, which were performed on four Markov 
ill 2.2 pi of formamide (83. S%) and EDTA blue- chains (die temperature of the chains and otiicr 
dextran loading dye (16.5%), heated at 95 C for [parameters were left at default values) with trees 
2 min., and immediately i^laced on ice. Se(|ueiiees sampled every 100 g(Mieralions. Markov chain con- 
were run on a polyaci") laniide gel on an API Piism vergeuee occurred rapidly (l)efore 2 X 10' genera- 
377 DNA se(]uencer (Applied Biosystems). C(ds tions), and 2000 trees (2 X 10' generations) were 


consisted of IP> g urea ultrapure grade [\ 
Solon, OH). 0.3 g A\mberlite mixed l>ed resin M15-loO 


hscaiiled as the 'T)uru-in 


f tl 

w process 

ss. Tl 


t * 

remauuug trees wen^ 

then used to construct a 50% 

(Sigma-Aldri(dK Milwaukee, Wl). 27 ml uanoptue majorily rule consensus tree, which provides estinia- 

waten and 3.6 ml Acryl/Bis (Amresco). 

[ions of each elade's posterior probability. As a control 
(lluelsenbeck et ak. 2002). four independent searches 

eini.()(;KM-:itc analysis 

\\ ere 

run, which vielded similar results. Ail saved 
trees from the independent runs (''burn-ins" excluded) 
Sequences were tulited and aligned in Scc]ueucher wei'c pooled lo obtain a consensus tree. Unlike 
version 3.1.2 (Ceiie Codes Corp., Ann Arl)ot\ Ml) bootstrap support values, posterior probabilities are 
(ollowed \)\ mamial optimization. Caps were inserted interpreted as true probabilities for each clade nndcr 
to keep the num])er of niformali\e characters (iudels the assunic^d [nodel (Rannala & Vang. 1996). 
and substitutions) to a minimum. Iudels were treated 
as unonlered. multistate charaeUus; thos(; ol etpial 
length that occurred in more llian one sequence were 
considered homologous and scored as separate binar) 
characters added to the data matrix. Insertions that 



Direct sequencing of the [jurified PCR pioducts 
yielded single l)an(ls on agarose gels and unambigu- 

had slightl) different sequences In two or more taxa ous ITS sequences (without oljvious muPiple bases), 

were treated as homologous (Barriel, 1994), and the showing no ev[dene(^ of paralogs of varying length, 

variable bases within these secjueuces were then re- The length of the sequences (iiududiug ITSl + 5.oS + 

coded as new characters (and treated as missing lor ITS2) ranged bom S90 base pairs (bp) (In Gueltdrda 

the taxa in which die insertions were absent). The data stcuophylld) to 609 bp (in GofKfilftgiiiud rosea), Tlie 

matrix is available from the lirsl author. aligned matrix comprises 680 positions (655 of which 

V heuristic parsimony search was performiul using represent the aligned secpiences and 25 die coding o( 

I^XLJP''' version 4.01b (Swofford, 1998), with 100 the indels, including autapomorphies). A total of 84 

random addition rej)1icatef^, 4'BR branch swa|)plng, sites were excluded from the analysis because their 

and MULPAPvS option In <-ffect. Relativ(^ levels of alignment was unc(M*tain (most of the indels present 

homo[)lasy and s\ uapomorph) in the data set were among lliese 81 positions were, liowever, retained in 

their reeoded form as indicated a])ove). Of these 596 

retention iud(^x (lU), and the rcscaled consistency characters intduded In the analysis, 421 were 

index (RC). as implemented in PALP'^ Tnternal const an 1. 76 variable but uniuformative, and 99 

brancdi sujiport was estimated with bootstrap analysis potentially informati\e. For two species {Guetidrdu 

(Felsensteln. 1985) usiug 1000 implicates with TBR hirsula and Piliunialis trichantha), 1TS2 sequences 

branch swapping and simple laxou addition. Pairwise could not be obtained. Clionielia spiaosa and (r. 

setiucnce divcrgeiu:e betw(,'en species ol core Cuet- stenopli yl I (i coiAil not l)e sequenced h.)r a region in the 

tardeae was calculatt^d widi PAIJP'^' ("p'' distau(;e, 5.8S eistron (1 7 and 19 ])p long. resj)ectively), and the 

calculated using llie consistency index (CI), tlie 

excluding ambiguously aligned sites). 

end of rfS2 could not be seqiuaiced for Timomus 

A Bavesian inference of phylogeny (Bl) was flaicsccus (16 nii>^ing l)p). In these cases, the bases 

obtained \\\\\\ the program MrBayes 3.0b4 (Ibudsen- 

w^ere treated as missing data. 


Annals of the 

Missouri Botanical Garden 

The 5.(!S cistroii is 165 lip in len<>-th (or all la\a. sonic (Inetlarda species (mostly from New Caledonia). 
except in llie se(|tience of Sh'iiosloiuinu niyrlifolmni 

and the West Indian laxa -W'olaugcrld and Slciioslo- 

provided hy Moynihan and Watson (2{K)1), whii-li is //////// seel. Slefwslomiuii. W^idnti diis second main 
2 hj) shorlei-. As often observed (e.g.. by Aiidreasen el chide, a weakly-snpported Pal(H^tropical dl 


ah, 1999; Moynihan <.K Watson, 2001), feu mutations sulndadc (P>S - 63%) nnites all the Paleotropical 

ucenr wtlhin this region. Tlu^ ITS 1 and 2 regions In species incdnded in ihe analysis except lywr [Guellfirdd 

the 40 species o( coce (hieltardeae iniduded \]\ onr spcciosa), \\\]\\c the Neolropical sulxdades (the first 

sani[)lt\ range in length from 213 to 223 and 207 (o comprising .Xeolaugrrln ami the second with Slcnos- 

221 hases, respeclively. Tlu'se h'ngllis hill vviihiii die lomiim seel. Slefioslo/nmn + (Uu'lUuda (irreund) are 

range reported for oilier angios|>ernis (I5ahl\\hi el ah. paraj)h\ Icl ic al the hasc oh the clade (ik* BS support). 

1995) and lor other gron|>s of Kiihiaceac (ATcDowidl i.K' 

Cucttdtdd a|)pears to he [lolyphylelic in our trees. \ 

Hrenier, l99o; Andreascn el ah, 1999; IVrsson, 2000; majority of the Neotropical taxa sampled iwv associ- 
Ka/afimandimhisoti Ov Hremer, 2002). Percent pair- aled with ihc Paleotropical t\pe species. G. spcriosa, 
wise distances l)et\\een i-ore (iucttardeae si)ecies and thus com|)rise the "(kicUanld s. sir." (dade (RS = 

range (rom lo 14.2 h)r ITS 1 (mean 
to 13.0 h.r ITS 2 (mean = 



2.4), 57%). The three I'cmaining species that occur in the 
5.3 ± 2.1). and to 9,8 New World are isolated (one is associated ^\ith 

Sk'/io.slo/diun lucidmn, while ihc other two ar<; pari 
amount of ITS variation is eomparahh' lo levels of die Bohni Clade) (Fig. 1). All lh(^ (tdicr Gucildrda 

\c g(Mius (Pahhvin el ah, species sampled occur in llie Old World and are 


.xO ± I..)) lor the whole hhS region. Tlii.-- 



y rc[M)i'ted lor a singl<^ ^ 

1995). sncdi as Vihuniiini L. (Donoghue »S: Baldwin. in(duded uidiin a Paleotropical Dioecious Clad(\ The 
1993; reviewed in Paldwin el ah, 1995) or infra- complexes of g<Micra usuall) associated w ith the three 

princi])al tnemhers of core Cnettard<*ae {GucKardd. 
(Porter. 199.3: reviewed in Pahlwin et ah. 1995). Anlirhcd. and Tininnius) are not evident in our trees. 
Comi)ared io other grouj)s of Ruhiaccae, variation Ouv limited sampling suggests ihat Ti/noiniis and 

generic iaxa such as Gilia sect. Gilidfidra A. ilvin 


'<i are fnonopin leiic and. ahhough often cousid- 

williin core (iuetianh'ae (ca. 500 species) is simihir lo 

(or in the case ol I hS I . lower than) that reported hy ered as close relatives, are placed in vei7 distant 



es in our trees. Anlirhea -h SleiiDsloninm 


Mtd)ouell and Bremer (199J!) for Kxi>s{cn\a (Ptas.) 

Ri(dL ex Ihiml). tS.^ Ronph (25 species), and similar to Aitfirhea s.h) is j)olyphyl(4ic, with Aiiliiiicd 

the levcd ohscrved h) Nepokroeff et ah (1999) within foiuunga paraphvltlic group with respecl to Tinfonins 

the main hn(>ages of Irihe Psy(diotriaeJ>ut inmdi lower and the New Cah^lonian GurHardd species in the 

than foi' the trib(^ as a whole (1000 in 1650 speci<\s). Paleotropical Dioecious Clade. while ihc meml)ers of 

The iVlJ* analysis yielded 1293 most parsimonious Sfcnosfdniiiin are repi'csentcd in two additional chides, 

= suggesliug it. too, may he i)ol)phyletic. 


riie 151 tr<u' is gi\en in the rii^lii half of Fiaur(^ 2. Its 


trees, (vich wiih a lengih of 415 (CI = 0.577, Rl = 

0.69.5. \\C = 0. 101). One of ihe shortest trees is ui^en 

ill Figure^ 1. The strict cons<Misns (Pig. 2) is W(dl ov(a-all topology is (|uiie similar to thai of the MR tree 

and the two analvsi^s essentuill) recover the same 
major (dad(^s. Moi-e (dades are well supported in llie \il 
analvsis (wilh [tosterior |)rol>ahilities exceeding 0.*)5) 

resolve(.l. although numerous (dades are not signiii- 

c-anily supported in tin* l)ooislra|) (RS) analvsis (HS 

50%). The ingrou|) node has strong support (15S 

99%) and the top(»logy al ihe hase of the irignmp is than in the MP analysis (some of wlii.di have BS 
fully resolved hut pooily supported, in contrast lo the values Ixdow 50%), hut those (dades thai are w(dl 
lerminal hraiudies. Fight pairs of spc^-ies iGiiclfdrdd su|)j)ort(Ml in the MP analvsis are likewise in llic HI 
diianv(it(i—G. eUiphcd. G, 7uninnrarj>({~G. slcnophylla, 
a knigu—a sp. ''(.adta," Slaioslomuin dcuhjfiuu—S. 
luvrtijoliuni. Bohca elailor-H. sdndnlcciisis. (r. crlspi- 

Irce. For example, the clade comprising New 
Caledonian Guetdinld and 3 Anfirhcd specit^s is 


strongly supported In the HI analvsis (posterior 

r<i~G, hirsufa. Timnuius nilidus-l\ polygdinus, prohahilltv, /' ^ 0.99), hut unsupp(a-led in the MP 

Ncoldiigcrui defisijlord-IS. icsinosii) receive high anaUsis (US < 5i)%). whereas the tdade comprisin 

l>ootstra|> support, ranging from 91 lo 100%. l^iiU)- G. diraricala and three other Neotropical GucUardd 

jiioiis is sister to lh(^ rest of the ingi-ou[), and the s()c(des has strong snj)porl in both MP an<l HI analyses 

remaindi'r o( ihc genera <'(trripi4se two main (dades. 




r. I 

- 1.00). The HI tree is slio-hlly less 
r(^solved than the Ml' consensus tree. ^eohntLtrrid 

The first ol these (dades contains mosi speci(\s of 

Giiclfardd, the majoiily ol the \cotropical genei'a. and appears sister lo th<^ rest of ihe ingrou[). whi(di forms 

the llavvaiiari endemic genus Rohca. Within this a j)olytomy of three elades. 'V\\v first of these (dades 

(dad(\ two (hirHdrda species ap|K'ar isolated as sisters encompasses mosI of the Ncolro|>ical genera, iii- 

o( Bobcd (comprising the "Bolfca (dade"). The second i hiding G\tctl<irdii s. sir.. Pillofildds and Mfjlaura (P 

major (dade com[)rises all the Pideotropical genera. 

0.5;); ihc second comprises the Bohca Clade [P 

Volume 93, Number 1 

Achille et al. 
Polyphyly in Guettarda 




Pittoniotis trichantha 


Matanea macrophylla 



Guettarda macrosperma 



Guettarda divaricata 

Guettarda eliiptica 

Guettarda pohliana 

Guettarda uruquensis 


Guettarda nannocarpa 

Guettarda stenophylla 



Guettarda combsii 


Guettarda pungens 

Guettarda scabra 


Guettarda speciosa I 

99 I— Guettarda krugii 

Guettarda sp. Cuba 



Stenostomum acutatum 

Stenostomum myrtifolium 

Chomelia spinosa I 

100 I — 

1 Bobea elatior 

Bobea sandwicensis 


Guettarda crispiflora 

Guettarda hirsuta 










Antirhea rhamnoides 

- Antirhea smithii 

Antirhea chinensis 

Guettarda splendens 



Guettarda heterosepala 



Guettarda noumeana 
Guettarda humboldtensis 

Guettarda trimera 

Timonius densi floras 





Timonius flavescens 


Timonius nitidus 

Timonius polygamus 





Timonius timon 

Antirhea borbonica 


Guettarda acreana 


Stenostomum lucidum 

Neolaugeria densiflora 

Neolaugeria resinosa 










5 Changes 

0.695) rcsulliti^ from 

Figure 1. ]^liylo<];rani oftnu; oi llic 1293 most paisiiiioiiiouri li'ccs (l(Miglh = 445; CI = 0.577; RI = 
ihc MP aiuil)sis (jf ITS (lala. NuDil^rrs on iiUeriiodes iiidicale l)(>(>ls|ra|) supporl (in %). GueUardu sprrics are in hohl. Type 
species of cuncnlly reeo^iiiz(Ml genera are placed in a hox; type s[)<'eies of genei'a currently })lat!ed in syiionyiuy are undiM-]ined 

(see lext for details). 


Annals of the 

Missouri Botanical Garden 















100 [ 





























MP tree 



Pittoniotis trichantha 

Malanea macro phy Ha 

Guettarda macrosperma 

Guettarda divan'cata 

Guettarda elliptica 
Guettarda pohliana 

Guettarda uruquensis 
Guettarda nannocarpa 
Guettarda stenoptiylla 

Guettarda combsii 
Guettarda pungens 

Guettarda scabra 

Guettarda speciosa 

Guettarda krugii 
Guettarda sp. Cuba 

Stenostomum acutatum 

Stenostomum myrtifolium 

Chomella spinosa 

Bobea efatior 
Bobea sandwicensis 

Guettarda crispiflora 
Guettarda hirsuta 

Antirhea chinensis 
Antirhea smithii 

Antirhea rhamnoides 
Guettarda heterosepala 

Guettarda sptendens 
Guettarda humbofdtensis 

Guettarda trimera 

Guettarda noumeana 

Timonius densiflorus 

Timonius tlavescens 

Timonius nitidus 

Timonius polygamus 

Timonius timon 
Antirhea borbonica 

Guettarda acreana 

Stenostomum lucidum 

Neolaugeria densiflora 
Neolaugeria resinosa 















1 r r iH 















Bl tree 

FigiiH' 2. C()iii|)aris()n of llic t'onsciisiis Irrrs (Voni llu- [\ll* n\u\ lil analvso of ITS dala. Tlio lice on lln- Icfl i> ilu- .slricl 
consrnsMs o! 129.'^ most p^usiriiniiious trees (iiuiiiIkts on i iitrinodos Indicate hootstrap \;i]ues o\ri- r){)%), Tlie tree on tlie ri^lil 
i,s llie SOCc niajoiit\ rule Bav(\sian consensus tree uudcv llie (/TH + I + F model of suhsliliil ion from four 2 X 10" -rencmtions 

■ ■ ■ O 

tuns (numlicrs on Inlei-nodes indicate postcrioi- [h oliahililit's). CueUardu species are in ImiM. (dad('s discussed in \\\v li^xl are 
indicated l>y d()ulilc lines. Geo^iapliic distn]>nlion of terminal ta\a is indieah-d as follows: ^rav = paleoliopical; dark ^r-av = 
Hawaii (Midemic; ii^^hl gra\ = en(]enm- to \e\v Caledonia: all i^llieis an^ ^^'otr-opical. 

Volume 93, Number 1 

Achille et al. 
Polyphyly in Guettarda 


0.92); and [hr lliitxl clade {P = O.HO), which is also lineage: G. noumeana ami an unnamed close ally (not 

recovered in the MP analysis, includes the type of sanii>led) have a dichasial cyniose inflorescence 

Steuoslomiim {S. lucidum), GiieUarrld acrrand. and the strnelure, and a recently discovered undescril)ed 

vvell-su])i)orted Pal(M)lropical Dioecious Clade [P = species (not sampled) has a dehiscent calyx ;vith 

0.99). Most of ihe smaller elades recovered in die BI circidar abscission. 

tree are also found in the MP tree, hul the position of 
PiUoniotis is inconsislenl between the two analyses. 

Within ihe GuelUuda s. str. clade, there are three 
main subclades. The lirsL comprises s[)ecies from 

Continental America (PS 

S%. P = 0.94). a few of 

DisCt SSiOA 

which, such as G. elliplica, extend slightly into the 
Carihbean Islands. Giiei tarda diraricaia, the type 
The poor support of the larger clad(\s identified in species iA DicrohotryiuJi VCilld. ex Roeni. & Schult., is 
\\w MP analysis (most with BS < 50% and none part of this clade. Members of this group are 
exceeding 63%) is unusual as ITS data are generally characterized by small- to medium-sized, nuMiibrana- 
most informative at sui)rageneric levels (Baldwin et ceous leaves, and possibly also by Uieir pollen (Fig. 2), 
al., 1995). For example, in a slud) of ^^ulguerIeae 
(Lantz et al., 2002), a similar-sized ruhiaceous tribe 


win en 

is similar to thai found in Aiiiirhea s. str. 
(()blat(!-spheroidal 3-eolporate pollen with reticulate 
(19 genera, ca. 600 species) that was examined using exine) (Achille, unpublished data). The second 
a comparable data set of 41 ingroup taxa. the major subclade imdudes two Caribbean species (BS = 

100%, P = ].()()), G. ruuinocarpa and Cr. sIcnophyUa, 
with veiT small uKMnbranaceous lea\'es, solitary 

elades are b(tth wtdl-resolved and strongly sup[K)rted. 
The sitnation found in Cnettardeae, with low support 
and/or resolution among the internal nodes, has also flowers, and small fruits. The diird subclade. while 

l)een observed in several odier grou[>s of liubiaceae. 
such asAliberlia \. Rich, ex DC. (P(M-sson, 2000) and 
tlie Catesbaeeae-Chiococceae complex (Motley et al.. 

57%. P 

0. /8), unites 

weakly supported (]?S 

a group of morpliologically distinct specdes mainly 

from the West Indies along with the Paleolropieal G. 

2005), as well as among groups of Asteraeeae spedosa, the type species. Guettarda scahra, the type 
([Baldwin & Sanderson, 1998; Carcia-Jacas et al., of Matlhiola (widely r(-arded as a generic synonym 
2001), Fabaceae (Allan ^ Porter, 2000), and Apiales .since Lamarck, 1792), also belongs to tins group and 

(Plunkett & Lowry- 2001; Chandler c^ Flunkett, 2004; closely resembles G. spevlasa. The fruits of laxa in this 

ihirtl subclade are rather large, as are the leaves, 
which are often coriaceous or bull ate and have 

Plunkett et al., 2004). This paltt^rn won 

Id 1 

consistent with a hypothesized rapid radiation early 

in a group's evolution, and cou 

1(1 (^xitlain the lack of scalariform venation. Guettarda pungens stands oul 

support at the base of our trees, which stands in 

within this group in having small, s{)in) leaves, and 

contrast to the morphological diversity thai has served small fruits. However, all members of U 



to segregate the core g(Miera within the tribe. 

porvi'iivrv of cvettmida 

Based on our analysis of ITS se(jnence data, 

subclade share a distinct pollen type, charact(nized 
by an oblate-spheroidal shape, 3 to 1 perorate 
aperlui'es, a perfoi'ated to reticidate tectum, and short 
columellae (Achille, uu|)ublished data). 

The inclusion of the widely distributed Indo-Pacilic 

even though the s|>ecles are morj)h()logieally quite 

Guettarda, as cnii-enlly circumscribed, is clearly species Guettarda speciosa in an otherwise strictly 

polyi)h}letic, with species distributed among four Neotropical clade is perhaps best ex|>lained by 

distinct cdades (Fig. 1). Most of the Neotropical relatively recent long-distance dispersal. Guettarda 

s[)eeies beloiig to the first of these, the Guettarda s. ^/^ec/ occurs in strand vegetation and coaxial forests 

str. clade (BS = 58%, /' = 0.91), which includes the on coral limestone, and its fruits have air-filled 

type species, (7. N/^, from the bido-Pacific region. cavities, making ihem well adapted to transport by 

'I1i(^ topology within this clade is well resolved (Fig. 2) ocean currents. This species is not found in Hawaii or 

the eastern Pacific, ahhough this may sim])ly reflect 

similar to one anotluM". Members of this group are the random nature of dispersal. It is perhaps more 

characterized b) usuall) globose fruits with more than sur[M-lsing to note that G, speciosa ap[)ears to be most 

2 locules. dichasial eymose infloresccMices (sometimes closely related to species from the West Indies (such 

reduced to a solitaiy flower), and a caducous calyx as the widespread coastal species G. ^'ca/>m mentioned 

with a circular abscission scar (Fig. 3). l^hese kist two above) rather than from the Pacific coast of the 

characters, although highly distinctive ol' Guettarda s. Americas, as one might expect. 

str., also occur (although not in combinatio!!) in three The second (dade containing members of Guettarda 

New Caledonian Guettarda species, where they may Includes two Neotropical sj^ecies (C. crispijlora and G, 

have evolved independ(Mitly from the con^ Neotropical lursula) that are riist(^r in our analysis to Bobea (BS < 


Annals of the 

Missouri Botanical Garden 




























.^ cT.'S 

v<^/ ,-^<f .c?\ ^A- 



^^ A' 


i Pii 




i Pii 




jPii Du Cp 


iPi: Du Cp 




H Cuatrecasasiodendron 
H Gonzalagunia 


An Du 

An Du 

An Du 

An Du 














H Pittoniotis trichantha 

H Malanea macrophylla 

H Guettarda macrosperma 

H Guettarda divaricata 

H Guettarda elhptica 

H Guettarda pohliana 

H Guettarda uruquensis 

H Guettarda nannocarpa 

H Guettarda stenophyffa 

H Guettarda combsii 

H Guettarda pungens 

H Guettarda scabra 

H Guettarda speciosa 

H Guettarda krugii 

H Guettarda sp. Cuba 

Pi ; Du Cp Ci H Stenostomum acutatum 


Pi: Du Cp Ci H Stenostomum myrtifolium 

An Du Cp Ci H Chomelia spinosa 

Cp Ci 
Cp C] 

Bobea elatior 

Bobea sandwicensis 

Du Cp Ci H Guettarda crispiffora 
Du Cp Ci H Guettarda hirsuta 

An Du Cp Ci 

An Du Cp C1 

An Du Cp C1 

An Du Cp Ci 

An Du Cp Cl 

An Du Cp Ci 

An Du Cp Ci 









Cp ffl 


Cp Cl 


Cp Cl 


Cp Cl 


Cp Cl 


Cp Cl 


Cp Cl 

Antirhea smithii 
Antirhea rhamnoides 

Antirhea chinensis 

Guettarda splendens 
Guettarda heterosepala 
Guettarda humboldtensis 

Guettarda trimera 

Guettarda noumeana 

Timonius densiflorus 
Timonius flavescens 
Timonius nitidus 
Timonius polygamus 
Timonius timon 

Antirhea borbonica 

An Du ? Cl H Guettarda acreana 

An Du Cp Cl H Stenostomum lucidum 

An Du Cp Cl H Neolaugeria densifiora 

An Du Cp Cl H Neolaugeria resinosa 























I'^igiuT 3. 

Important nioqiiiological chamrlris maf)i){_M.I on llir 30% luajoiilv inic Ravcsian cons.Misus iicc. Ninnl)crs on 
in[<TMO(lcs indicah^ poslcriof j)rol>;iliilitics. GueUnrdn sprcios arc in Ijolil. Tln' .svml)()ls indicalr llu' slalc for cacli raU'^ory of 
cliaraclers (Pollni lv|)(': Ti = Pitfoniolis; An = Anlu'hea: {]\\ ^ CueUardn: \\u = 


. '; 

)i'ir. : — ntiknown. Fnnl t\]>r: Cv = 
capsular; Du = diLipaccmis with unilcd [)>n'n('.s; \){ = dnipaccous uiUi frre pMvnrs. Calvx Ivjio; Cc = cadiirous !)v 
abscission; Cp = porsislcnt on fVinl; ? =- \anabk-. lidloiv.-rctu-c lype: ]'n = paniculate; (:2 = rundain(!nlall\ dicliasial c\u]c: 
Cl = fundamentally tnotiocliasial cyme. S(^xna] system: H = hcnnapln-odilism; D - dioiH*y). 

Volume 93, Number 1 

Achille at al. 
Polyphyly in Guettarda 


50%, P 

0.92). Those la\a exhibit several as IriineroiLs flowers, corollas with valvate reduplicate 

(h.-.tiiictive cliaraclcrs that separate them from other aestivation, and a woody endocarp with up to 20 

llier locules. The lack of resolution within this clade 

members of (lucUnrda. Along wnn a lew o 




apparenLly closely related species from Central and reflects a high level of similarity in the ITS sequences 

South America that were not sam|)led, tliev form of the species sampled. In another study of ca. 20 

a well-defined group characterized by large stipules species from New Caledonia and snriouuding areas 

with membranaceous mai-gins, scalariforni \enahon, (Achille iS." Motley, unpublished), we found that the 

ifid monochasial Infloreseences (which (h'Ifer from se(|ucnces are idenlical or differed by only a few 

llie dichasial cymes found in other Ncolnjpical bases, suggesting that this clade may comprise 

Cueitnrdd). small 4-ribbed ovoid fruits with a minute a closely related grouj) within which ra|)id morplio- 

and persistent cal}x (see also species descriptions in, logical di\ersifieation has taken place. perha])s in 

e.g., Standley, 193 k Steyermark. 1972: Taylor et ah. a mamier analogous to that observed within Guettar- 

2001), as well as '^Bohca type'' pollen (see below deae as a whole. The pattern of diversification 

under So/>c^/). Altlu)Ugh additional molecular dala will appaixMit among the New Caledonian sp(M'ies differs 
be required to confirm whetluM- ihese taxa and Bobea 
arc closel) related, their distinctive morpholcjgical 
characters suggest that recognition at tlie generic rank 

substantially from that 

of die mostly Neotropical 
Guclidrdd s. str. clade, wh(M-e resolulion is better and 
blanches are longer (Fig. 1), even though there is 

miglit be in order, in w 




le name 

com[tarati\elY little morphological variability anion 


Tourneforiiop.sis woulfl be available, as it is typified its members. In order to evaluate a hypothesized 

by T. rcliculala Husby. (= Cnctlarda toururforlinpsis 
(Rushy) Standi.), a close relative o\' (t. nispijloni. 

ladialion centered on New Caledonia, it v\ould first be 

necessary to sample achlilional species of Anfirhcd 

The Cue!t<srd(i species from New Caledonia cotr-ti- snlig. Cnelinrdtdla and snbg. Mesonirpa (sensu Chaw 

lute a third clade (Fig. 2) that is ver) w(dl >upported in 
the Bl analysis (P — 0.99) altliough unsup])ortcd in 

2). the apparent closest relatives of 

tlie MP analysis (BS 

50%), This clade includes 

& Darwin. 

New Caledonia Guclldrdd. according to olu" results. 

Tlu^se subgenera are most divers! I led in Soudieasl 

[]u-ee^i^cw^ n{ \!!lirhea{A. cluncnsls^A, rhaninuulc's. Asia, but we were able to include only one specie's 

fiom Soulli China {Andrliea chincnsis). one from Fiji 
(.4. snillldi), and one from New (Caledonia (.4. 


and A. smilhii) that would either belong to nie 
segregate genus Giietlardclla according to Jansen 
(1984) or [o Andrhea subg. CucllardeUa and Inlirlwd rlianinoides). 

subiT. Mes 

^. mesocurpd aceoranig 


to Chaw and Darw in 

44u^ fourth grou[) of Ciietlarda identified in our 

(1992). Tins (4ade is nested within a l)roader stnd\ comprises a single species, G. armuui, which 
Paleotropical Dioecious Clade (see below), and is api)cars as sister to Stenostomum hicidum. This w(41 

known (liicUdrda^ \Nid(4v distributed in northern Soutli 

the sister irronp (if Timonius. The Ne\v Caledotnan 

s[)ecies ni' GucHarda are morphologically very dislim-t America, was sampled in olu" analysis because of its 
from the Neotropical membta-s (tf the genus and from distiticlixc morphology, particularly its calyx, whu-li is 
G. speciosa. In fact, several characters, inchuling mostly caducous but not shed by abscission. Its 

dioecism, a calyx that is almost always persistent in 
fruit, and monochasial cymes (Fig. 3). are r(Mnini>ccnt 

affinities are discussed below under S!idii)s{o7nunu 
Our finding of pohph\ly in CucUarda Is coir-istcnt 

oi Antivhea s.l. The placement of these species williin w4tli moiphological data, as several nnitpie characters 

the Paleotropical Dioecious Clade is thus consislent 

are associated with each of the chides revealed in our 

with mor[)hology, and their inclusion in a liroadly analysis (Fig. 3). GiicUdnld s. str. can be recognized 
defined Guelldrda bv Baillnn (1879), Cnillaumin by its caducous calyx, which appears to be a synapo- 

(1948). and more recendy Jalfre et ah (20()4| merely mor[>h\ for the lineage. Ilowevei 



has I 

)een some 

confusion belween what we regard as a truly caducous 

reflects an out-of-date concept of the genus that has 

been abandoned in most other parts of the world. It calyx (shed by abscission) and a calyx that is minute 

or lost as it disintegrates (without leaving an evident 
af>scission scar), as seen in C crisj)ijjnrd, w4iich lias 

therefore would seem ap[iro[)rlate to exclude the New 
Caledonian species from Guelldrda and transfer them 

to another genus (see discussion below under been misinterprelcd by se\eral authors (e.g., Dwyer, 

1980; Standlev. 1931. 1934; Standley & ^\411iams, 
1973; Steyermark, 1974). Species of GhomcUd have 
Caledonian Guelldrda clade is very weak despite the also Ix^en re[)orted to possess both a de<'iduous and 

persistent calyx (Purger & Taylor. 1 993), but 

It is worth noting that the resolution within the New 

fact that its members are morphologically quite 

distinct frorTi one anodier. Many New Caledonian additional developmenlal studies will be required to 
species of Guellarda show one or more characters that evaluate whether the nature of the calyx in this genus 
are rare or unknown elsewhere in Cuettardeae, such is homologous with thai seen in Guelldrda s. str. Our 


Annals of the 

Missouri Botanical Garden 

molci'Lilur sUuly docs not j)rovi(le any evidence of Haw;iiiaii g<Mitis Holwa is not eoiiriniied hy our 

a close relationsliip helweeti the lv|)e sjKM-ies of residts, des[]ite the fact llial ihc) are hutli di(»eeious, 

Clioniclid and CucUarda. as eintentlv eireL]iiiseril)ed. a eliaraeler found dn-ou^lionl ihe Paleojropieal clade, 

and ihat tlie\ share (ree pyi'enes, which are \\i)\ known 

mor[>holo<^u-al di^lniction hctweeji dietn ixanalns an\ wliere else in I he lrll)e. Tnnonius is fnrdicr 
unsalislactury. \\ ith our more diorongh sanij)hng, it 
also a|)])ears thai the assoeiaEion of ClionieJ'ui with (I. 


h. . 

even inongn. aeeording lo Taylor el ah (20(11), \\\c 

dislincli\'e among 

lUihiaceae heeanse of its largt 



nmh(M- ol o\ary locades, which can exceed 500 i 
rrispiflord snggested l)_\ Ho\a <■! al. (2002) may not some species (Darwin, 190 1), whereas mo^t memhcr^> 
rellecl a close r^dationship hetu<^en \\\v two genera In of the family have hiloi-ular ovaries. However, sev(;ral 
llicir stiicler s(Mise and tlins does not snpport [\\v, olhei- groups also -how increases (albeit iimeh morv 
in(dnsion of Chonwlla with mi Guelinrdd s, str. (as 
defined here). 

modest) in locale number, incdnding some Neotrop- 
ical CneUnnJiU Bohcd, and most 


nieniners o 

f the 

Fnilher analyses w dl he iiecessan before e\teiisi\(^ Paleot ropical Dioecious Cladr-. Thus, ahhiou'di cliar- 

acters of ilu; g)n(»eeium are usual I > considered 

tlie most im[iortan( in infra familial classi- 


nomcntdatural (dianges can be made vvilhin (kicUarda 
sd.. as most of tlu' larger elade> identified in our stnd\ 
are insid(iciend)' su[)porled in the Ml* boot^traf) atid fication of Knbiaceae, it seems very Iik(d> thai an 
HI analyses, and broader sampling is needed for some incacase in ihe nunibei- (^f huades has occairrcd sev^eral 
f tluMii. It u(uil(h however, seetn a|)propriate [o times in(lep(Mulently \\itlnn Cuetfardcae, although 


)e may 

incages ni whitdi il 

exclude die New (Caledonia species Irom (luclUirdu, the evokuion of this (diaracUu" within the Iril 
whitdi (dearl) constitute a group that is distinct from not \)C strictlv homologous in llu 
all other ineni])ers of the genus, as currcjitly 

circumscribe<l. and in parli(adar fiom the tvpt; 
speides. C. spcciosa. 


lougli numerous g<ai(a-a and sj)e(aes 

OTiii'.K (,i:M:ii \ or eoin-: f:t KTi\in)i:At:: 

l{tdationslii|)s williin core (uieltardt^ae. as within 
(juelhirdd. a|)pear well corndated widi geogra])hv. All 

AiUirhcd, iW{\ 
hav e been assotdated w ith or incduded in A/ilirhr<i. oui- 
data suggest that a restricted generic cir(amiscrij)li(Mi 
ma} be approj)riate. ddic inoiiot\pic Neotropical gtaiiis 
PilloniolLs has somelimes be(ai in(duded in Anlirl 
(e.g., by Dwyer, lOJSO), but ntdlhcr of our trees 
provides evideaice for a (dose relalionshij^ wilh either 


the Paleolropical species sampled, except the llawai- Anlirhm or the previously incduded Neotropical 
laji taxa ami llie w idespread eoaslal specdes C. 

speciosa, belong lo a Pal(Mitro[)ical Dioecious Clade 



Slcnuslomini! (Fig- 2). 



basis traditionallv invoked for ibis 

thai Is wed snpporlcd in the HT analysis (/^ - 0.90; pulalive relalionship is rather weak, essentiallv 

I'dg. 2). Since the cdosesl allies of tl 


' genera 

i mi ted to die pres(aiee In both Pitfaniods and 

comprising core Guellardeae are Neotropical (Bremer, Aiitirhca of cal 

yx-crown(Ml {lrup(\s wilh few uniled 

1996; Ur.Mncr.Kdludni. lOOii: Kovaet ab. 2002). this pynaies, characters tlial are In fact (airlv 


su^i:<\sts a N(^w ^\)rld orliiiu 

for the grou|), a\ ith 
presumably h\o scpai'ate ev<mts involving dispersal 

(or \!cariance) to account for the presence in the Old 
World ol the Paleotropical Di(K'(dou-'^ (dade and of G. 
sj)ecu)S(i. Dioecy eharacleri/es all members of the 

within (.'ore (.uetlai*lea(\ PiUofiiolis differs, how('\(a'. 


in several ImportanI vvavs, sutdi as having paniiadate 
inllorescences. exseited stamens, and distinctive 
prolate 3-colporate |)ollcn uitli perfoialc cxinc (the 
lattta- (ealure oe(Mn-ing al^) in Slenostonitini seel. 

Paleotropical Dioendous Clade, viz. Timnidus, Anti- /?e.v//;.//?///;/,v Hnrlii(li. repn-scaitecl m our analysis by N. 

rhca and llie N(w\ (ialedonian Cui'lUirda specdes, in 

i-ontrast lo other core Guettardeae. whose sexual 
system is almost always heiniaplircMlitism, the otd) 
exce[)tion bcdug the dioecious Hawaiian endemic 

(liiildliun and S. myrlifoliuin). wliereas Anlirhca has 

4 ■ 

nionochasial cvmes. Included statncns. and oblate- 
spheioidal .'^-colporale pollen with r(4icadate exine 


(dnile, unpublished data). All llie dislinetive 
genus H<d)r<i (cated as jiolvgamodioctdous by Darwin fealurc^s of riUnniufis menlloncMJ above arc^ shared 

wilh Midiiucd (Fig. 3), but occur nowhere cdse within 

used ni this 

& Chaw^ 1990). 

Tinionhis. DespiU^ the presence of cunsidca-ablc core Cuetlardeae (ihe outgroui) taxa 
inor[du>logical heterogeneity within Tummius (Wong, sludv, howe\<M-, exhibll some of them; Acdnlle, |)ei-s. 

obs.). ddiis suggests an afflrnly between Puioniolis 

gcams IS easil) 

distinguished among 



J 988). Ibis 

Paleolro|)ical Cuettaiilcae b\ its frec^ pyrcaies. ddic and Mdldrica thai 

five specdes Incduded ni our sample form a claclc^ that sister relalionship indicalc-d by ihe \\\ analvsis {P 

is wcdl snpporlcMl in die HI analvsis {P = TOO), but 0.85). 

le eongrncait w ith ihc 

Old) weaklv so in ihe VIP anal)sis (ITS - 60%). The 
uotioii thai Tnuon'nis Is rcdated lo ihe endennc 

ddie I rS data clearl) indicate that Aiilirlicd sd. (i.c\, 
incdnding Slcdosloniun}) is j)olv])hvletic. Kven the 

Volume 93, Number 1 

Achille et al. 
Polyphyly in Guettarda 


more reslrictcMl definition of the giMius projiosed by Caledonian species aiv morpliologieally (luite varuiM 



lifferent \vnm I hose ciiiienuy nieiuuec 

lIv ineluded i 



a n d 

Steuostomum. Our residls suggest ihat Sleno- 

Chaw and Darwin (1992), who ineluded only the 
Pal(H)lropieal s[)eeies hut excluded Stenostomum, 
aiijx'ars to be parapliylelic with respect to Paleolrop- 
ical members of Guetldrda and Timouius. Our slomam may also be polypliyletic, with S. hicuhun iti 

a weakly supported sister relationship to Cuetlarda 

= 52%, P = 0.89) and two odier species 

samphng, w^iile modest, suggests that in ordfM- to 
render Aiitirhea sensu Chaw and Danviu (1992) 



monophyletic, it would be necessary to include both [S. aculalum and S. myrtifoliiuu) forming a separate 

Timonius and the New Caledonia species of Guel- dade (BS = 94%, /'= 1.00} tluit is sister to C/K>/^?c//a 

tardd. [f sucli a broad defiiulion were used, AiiUrhca [n the MP analysis (BS ^ 52%). As meulioued af)Ove, 

would constitute a very larg(^ genus (comprising about Borhifh and Fernandez (199.3-1991) placed 5. 

230 species) that corresponds more or h^ss to lucldum in Sleno-slonium sect. Slenostnnunn, Avhereas 

Schlcchler's (1906) broad conce[)t of Tunonius, the otlier two species in our sample belong to their 

Adopting such a circumscription would, however, section Resinarithiis. Our study supports the idea that 


ako it verv (hfficuh to define Anlirhea based on 


lese two groups are 

distinct, as suggested I 

mor|>liological characteis and thus does not seem morphology (Rorbi{b & Fernandez, 1993-1994), l>ut 
advisable. their placement in different |)arls of our trees would 

It would thereh)re secan best to hniit Anhrhea to 

not be consistent widi maintaining them as a single 

species from 

the luihau Ocean, com|)iising A. genus. Tbc possibh- sister relationship of G, arrcana 


borhonica (the Ivpe species) and two (dose rtdatives l<» the tyi)e species n[ Stenoslonuwi, although weaki) 

{A. hijurcatd (Desf.) Hook, and A. madagascnricnsis sup])ortcd in our trees, would on the other hand be 

Chaw), whicb together correspond to Aniiriica sensu consistent with morphology, as several characters 

Janstai (1984), ov Aiiiirhea subg. Anlirhea sensu Chaw shared l>ctween tliese taxa ((;.g-, siuuhu" iunorescence 

and Danviii (1992). In our analysis, this group structure, small ovoid fruits, and a caly\ that is not 

(rc^prescnted by A, borhonicn only) is sister to all the shed by abscission) are not found in members of 
other Paleoti-o])ical Cueltardeac (BS = 63%, /-' 

Gaellarda s. str. For exampl(^ Bremekamp (1959), 
0.99). A more narrowly defined Anlirhea would be who w^is familiar with Slenoslonium (under the name 
easily characterized l.>y its mononiorphic male and Anlirhea) in Central America and tlie West ln(hes, 
female inflorescences (i.e., whi{4i have similar while studying an undetermined specimen of G. 

arreana collected in Surinam, recognl/ed it as an 

branching patterns), ovaries with only 2 or 3(4) 

locuh^s. and the presence of crystals In ihe leaf Anlirhea. He consequently did not suspect any 


If this narrower interpretation ol Anlirhea is 

relation of liis specimen to Gaellarda and described 
it as a new species, A. surinaniensis Bremek. It might 

for tl 

le species oeionguig 


lo Anlirhea subg. Guellar- 

adopled a n(^w generic placement would be needed thus pro\e appro|>rIatr to include the Soudi American 

G, arreana within Slenostomiini, a relationship that 
della (represented in our study by A. chinensis, the cariier authors (e.g., Steyermark, 1972) perhaps 
type species of Guellardella, and by A. rhamnaides) overiooked simply because Slenoslonuun occurs 

and Anlirhea su])g. Mesorarpa (represented by A. 
smilhii). Chaw and Darwin (1992) recogni/cd l)()th 
these subgenera, which together formed a clade in 1993-1994). 

farther to the north, from the 

West Indies to 


thern Central America (Borhidi <!l' Fernandez, 

Despite being well distinguished by having stipules 
united into a sheath, Neolauu^erla was merged into 

their analysis. The first subgenus com[)riscs species 

mostly from Malesia, Southeast Asia, and the 

southwest Pacific with small 3- to n-locular fruits, Slenoslnwum (as a third section) by Borhidi and 

and the second includes Melanesian species w^itli Fernandez (1993-1994). We are unable to confirm 

laro-e, 8- to 16-locular fruits. Taken tog(4hci 


this this inter[iretation. as the two species of Neolaugeria 

in uur sample (which comprise a well supported pair, 
BS = 100%, P = 1.00) form a paraphyletic group 
taxa. As the New Caledonian species of w ith the S. ///r/r///;?M-lade in ihc MP tree, whereas they 
Guellarda may belong to die same broad clade as api^ear as sister to the rest of the ingroup in the BI 

tree, ahhoui!:h both toi>ologies are uusup|)orted (BS 

group corresponds lo Gaeltardella sensu Jansen 
(1981), which could be resurrected to accommodate 



the GueUardella group (BS < 50%, P = 0.99), they 

could perhaps also be iuiduded in an even more 50%, P = 0.63). Moyuihan and Watson (2001) also 

broadly defined GueUardella, If Uiis relationship is rejected the iiudusiim of A^tW^u-ma in Sto?05fo7nn;7? 

and a substantially using ITS sequence data. Their results were, however, 



confirmed by future 

enlarged GueUardella is recognized, il would, how^ev- based on an anal}^is that includ.^d only one species of 
er, constitute a heterogeneous group, since the New Stenoslonaun, 5. uiyrlifolLum. a member of section 


Annals of the 

Missouri Botanical Garden 




fianufiis, wnich in ouj- study was res()l\('(! iii 

Ceiihal and Soiill) Anicrira and (Ik* Coc-os Islands 

rallici- ihan a wcslcrn racific oriiiin. a: 

s nnpiieu ny 

1 I 

I tini 

a cladi; distant from [lie NeolaugerUt group. 

Swnosloinum has Ixt-r consich'n'd a syiioiiun of a tiach'lionally assumed relationship to llie l^deotrop- 

A/in'rhea l»y sonic aulhors (e.g., Schumann, 1801: ioal Timmnus. W Bobca is Indeed derived f 
Standley. 1934; Hreniekami), 1966; Airy Shaw, 1973; " a Neo|ro|)ieal ancestor, its dio(rv ma} hav(^ evolv(Ml 

Sleyermark, 1971; Roljhrechl, 1988) hecaust; diese independently from ihe Pnh-otropieal l)i 

luo gen(M-a are niorphologieally sinular in s(^veral Clade, perhaps as an adaptation to an insuh 

aspects (e.g., nionocliasial cytTies, a stony endoi-arp eiivironmenL a pattern thai is seen m many other 



olten with feu locuL^s, and a persistent calyx). Oni 
resiihs suggest that the type species ui Slcnosd^nium 

Hawaiian groups (Sakai ct al, 1995). Hawaii has one 
of [he highest incidences of (hoecy (14.7%) of any 

is indeed closely rehiled [oAnlirhrn, and in particular Hora in the worhl, and many (hoeeious lineages arc 
to A. hurhnnica (the type of that genus), although derived from dimorphic ancestors, which was d.on-hl 
phiced sisUM- to the Palcolropical clade. Our data art 
thus consistent with Chaw and Darwin's 

sugg<\stion dial Slrnoslofnuni 

1 992) 

is best treal(Ml as 

a (hsliuct ii(^nus. 

Bohea. Tlie exclusion oi' the Hawaiii 

to he die case foj' Bohea (Sakai et ah, 1995). Bobca 
may thus l)e a 13lh Hawaiian lineage that is believed 
lo have evolved dioecy from hermaphrothtic colonists 

(Sakai et ah, 1995). 



ui genus 


Cii I rum Cuettardeae was pr(t])osed by J\ova 
(1999), bul l)oth our analyses sugg(;st thai Bobca is 
nesl(Ml well within the uibc (BS ^ 99% and P - 
1.00). KurtheruKtre, ihe placement of Bobca within 
eore Cueltardcae has long been recognized based on 
morphological ieatiuvs. />oAea luu 

characters in eomtnon with other genera of core a group of sjiccies characterized b\ dlchasial 
Cuettardeae, including typically seeund, monoehasial (somelimes reduced to solitary flowers) and a caduc( 
mflorescenees ihal are once-dicholomous al the ba^e; calyx with a circuhir abscissi(.n /one, which is w(dl- 
fleshy Iruits with numerous similarly-struclured (hversified in lh<^ Neotropics, but also comprises 

Olh- stud}', using a broad sam[)ling that repr(\si'nls 

most o( the morphological and geographical diversity 

within Gucllarda, indicates llial die genus is pol)- 

AS numcn)us ph)h-lic. Cncdarda should piobably be reslricted to 


► us 

|)vrencs; elongate cylindrical scf^is widi small 

ct)ly]edons and !o|)p(Ml b) an obturator; and overall 

vcg(4ative aiid floial morphology whidt chjscly 

resembles some species i){ Aniuhca, GucUarda, and Anlirhca-GuclUirdclla complex, whose internal rela- 

Tummnis. The position of Bobca in ihe tree presented lionshijis are in need of hirther sludy. Our results also 

by l!o\a (1999) thus seems at odds willi bodi ITS data indicate that stweral morpholo^dcalb distinclive 

a single widespread species in ihe Paleotro]Hcs. Tlit 
numerous endeniii; New Caledonian species currenMy 
assigned lo Gucttarda clearly Ixdong to a distinct 

and mor])hology, suggcsling thai Ivova^s [ilacemcnt 

INeolropical speci(^s Iradilionall) inchuhMl in G'//e/- 

may have resulted fn>m an error in samj)ling or tarda are |)laced outside Guelfarda s. str.. although 


\\ itliin core Gneltanh^ae, Boltca does tiol appear to 
bt^ closely related to Timonias, despite the faci diat 
these two genera were once tousidcred as svnorn rns 
(Candolh^ 1830) or, more nnn^ndy, as (do: 

theii' exact alfinilies remain miclear. 

Our study also pro\ ides some intei-esting insights 
cont-iMiiing the delimitations of other g(Miera in core 
(Tuctlar-d(\ie and the distribution of characttMs within 

the [v\hc. Our data confirm that ihc Neotropical genus 
(Darwin iK Chaw, 1990). On the contrary, as indicated Slcnoslomuin is distinct fn.m Anh'rhca. which should 
earl i(M\ /?o/;ra niay instead b(' sister I. > C;. rm/;(:/^/7/ + dius be considered as strictly limited to die Old 

World. Kurthermore. Aniirhca and S!cf}os!o//nini both 

se allies 

G. Inrsuta, thus forming the Rohca Clad(\ altlutu'di 
tins relationship is weakly supp( tried in the HI 
analy^^is [P = 0.92) and unsupported In the MP tree apidicalion of n^ 

(Kig. 2). Il is worlh noling, however, that all of thcM- 

appear lo be po]yph\letic and may thus re(|Lnre the 

niowed generic circnnrseri])tions. 

Fealm-cs of the gynoecium (such as ih* 


numner o 


sp(M'i(^s are well-charact<M-ized (Fig. 3) by ihe presence locnies and fusion of the ]nTcncs), which ha^e often 

ol "Bobca type'* pollen (s|>heroidal porate [)()lh'n wilh 
very thick, retieulat(^ exine; Aclnlle, unpublislKMl 

been coiiMdert^d among die most ifupoitant characters 
for r(M-ognizing sn[)rageneric taxa williin Ivubiaceac, 

data), wliich appears lo be unlciue In th.' tribe, and do not appear to be particularl> well correlated with 

also by their innorescenee structure (bifid mono- the groups idtmlificd in om" analvsis. Several in- 

ehasial cymes), di>[inctive from Gucilarda s. str. A teresling correlations have, however, been found 

New World (.rigin of Pu^Jh'u may thus be plausible, IxMwcen our phylogen) based on ITS data atul llu^ 

snice G. rrispljloni and its rehilives arc di^tribulcd in di.^tribution of cerlain previoii>ly-i^. 

Ihe Ni-otropics and In parllcularon du' Pacific coast of utilized characters. For example, a lai 



^noreo or undcr- 
■ge Paleolroj)it:al 

Volume 93, Number 1 

Achille et al. 
Polyphyly in Guettarda 


Dioocious Clade is characteri/cd hy ils (lislijirtive B.-rhidi, A. & M. /. Fcnuindc/. 1993-IWi []9%|. The 

sexual syslein. Tlic recognition of sc^'eral [xdlen t}pes 
among the niend)(as of core Ciieltardeae, and llie 
homogeneity in pollen type seen within several clades 
identified in our pliylugeny, also suggest that 
palynological characters may he Vcduahle for fuillua" 
sliuhes at the generic andAjr specific levels within the 
trihe. Finady, with regard to biogeogra])hY, although 
Guellarda sd. and AtU'irhca sd. have generally been 
considered to show trans-Pacific distril)utions \\\\\\ 
Iwo disjinict areas of diversification, one in tlie Old 
^"orld and another in the Ne(»tropics, our study 
suggests tliat this iiiterpnMation was erroneousl\ hased 
on iion-nionophyhHic generic concepts. 

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Mo)nihan..I. X L. F7 Watson. 200L IMn loi^eo^M-aoln trenerie 
aliies, and nomcnclalnre nf Garihheau endemic genns 
Ncoldiigcrid (Kuhiarrae), hascnl on ITS se({u(aiees. InL J. 
PL Sei. 162: 393-10 L 

Mueller, \\ 1875. FragmiMita Phytographiae Austrahao: 9, 

Nepoknu-ff. M., B. Bremer & l\. J. Svlsma. 1999. Re- T. 
orgaiii/atiou of the genus Psycholria and trlhr Psycholriae 
(Rnhiaeeae) inferred from ITS and rbvL s<'(iuene<- dala. 
Sysl. Bol. 21: .5-27. 

Nvlander, J. A. A. 200 L MrModeltesl 

tl L. 0. Williams. 1945. Flora nf Guatemala — 

l{ul)iaceae. Fieldiana: Bol. 24: 1-275. 

Steyermark. J. \. 1972. Rnhiaeeae. !'[»■ 237-8.32 /// B. 
Maguire c^ eollahoralors (c<lilois), Bolaii} of the Cuayana 
Higldan(Ls. Part. IX. Mem. Ne\s ^ ork Bot. Ganl. 23.' 

. 1974. Kuhiaceae. (hieltardeae. V\). 772-867 in T. 

\2. Proirratn 

distilhnted h) the anihor. Evohitionarv Bioh»<iy Genlre, 

Uppsala Universttv. <htlp:/A\\\\\ \ ah -Ion. T. 1909. 

Lasser <.^ J. A. Ste\<-rmark (edilctrsl Flora de \'cn(vai(Tt 9. 
Sunfford. n. L. 1998. PALP='=: Pli)h,genetic A>ialyshs Using 
Pai-siniony (='= and oilier melhods), m-w I.Oh 1 . Sinauer. 
Sunderland, Massac husells. 

I) lor, G. M., J. A. Stc:yermark, P. G. l)elpr<-te. A. 
\'inc<-nliu[, \\. Corles, 1). /appi. G. Perssou, G. B(;slelli 
(^osta X E. yVraujo da Anunciavao. 2001. Kuhiaceae. 
Pp. 197-847 /n J. A.StcNcrmark. P. Berrv. K. ^alskicwch 
& B. ilolsl (editors), Flora of ihe Venezuelan Gua\ana, 
\y)\. 8. Missouri Botanical Garde-- ^^•• 

n Press. St. Louis. 

Boiirage zuj 

Kennlniss del" Gatlung 
Tinutniits. Bulh Hcpt. Agric. Ind. NeriT 26: 1-61. 

Volume 93, Number 1 Achilla et al. 


Polyphyly in Guettarda 


VcrdrOLirt, B. 1958. Remarks on the classifieatinn of tlie D. Gellaiid. J. Siiin^ky & T. '«1iitc (editors). PCR 

[^ul.iaeeae. Hull. .Tard. Bot. Elal 2,".: 209-281. protocols: A Guide to Metlu»ds and \ppHeations. Aea- 

Wliile, T. j.. T. Bruns. S. Lcc & .1. Ta>lor. 1990. demic Press, San Diego. 

Amplificalion and direc't sequeneing of fungal rii.osonud Wong. K. M. 1988. The Aniirheuideae (I{nhiaceue) of ihe 

RNA genes fur ph) logiMietirs. Pp. 3 1 .5-;^22 //) M. Liiuiis, Malay Peninsula. Keu Bull. 1:5: 191-.'5l8. 


Ciisluia Inocencio,^ Diego Rlieni,-'' 

M" Coiicepcion Ohchi,^ Frdudsco Alcuniz. 
and Jose-Anlomo Barrcna^ 



A systciiKitic rvvisioM iA' Cnpparis seel. Capparis. froni wrsl<MH atul (:('MLial Asia, Noilli Afrira, and Kiirnpc, is [)r('sc.ii(Ml 
\\vvi\ Ilic taxuiUHin ol lliis s(H-ti()ii has 1 


'^ '*^*'" 'ippn)ac!i.Hl <M»iiil]iii!ng nmrpholo^iral, hio^t'o-^iaphifal and ia..I<-culai- dala uhcii 
avadahi.^ Ten sp.rics aiv rcvo-iiiz.-.l. iruludlii- tun nrw s|H-.-ics, Capparis a/fanfira and C. zoharyi. In addilion, four new 
snhsprcios are pivscnU^d: Cappari.s uvula snl>s,). m)rlifoliu, C. pamJJum .nhsp. sphurmrurpu. C. siaila Mihsp. nwsopolumiru, 

Uipticu, C. 
iilu siiltsp. 

and C. Simla snl)sp. .snuliuna. Led, .l\ pes are designal.-d for C. ueg)pliu, C. licrcrucusis. C. niunrmifulia, C. r 
nnurunt'Julia Boiss. snhsp. rusanurianu, C. rupestris, C. orala, (I purrijloru, C. v..r. cuncscens, C ,s/r.,., 
hrrhuccu, and C. sicula suhsp. InuuphvIIu. \ full taxononile tiealtnenl. kevs, and disl [ II mlion maps of llu- .-eeoon[/,(.<] 

an^ provided. Hie hvo new species are illiislraled. 
ki'Y irnnis: (_;aj>paraeeae, ('<ippuris. laxonuiuy. 


Ciipparis (K7.7:7r7.pic) is a name coiiuMl l)\ dlu^o- 

lransf(MTcJ lo sctTiun Monoslirhocalyx l^adlk. and 
seclion Hushcckea (Faull.) Benlli. i.K Hook. Sid)seelion 

II series on 

plirastns (Ith e<'ntnr\ HC) and endorsi'd hy Uioseor- 

idps (Lsl ecnlurv AD). Il s(M'ins to have eoine into widf^ Srriales DC. Kaeetnose lid'loiVM-ence.s or i 

use after die spread of llie Arab culture in the Middle the stems. Repre^enlalive species: C. zeylanica L., C. 

Ages. T\w Genus Capparis uas created hv Linnaeus aanninala W illd.. C. quadrifJora DC C. roliindilolia 

(1 ^S:?. 1/5 1) with ih.' description of Capparis spinasa Kottl., C hrvvispina DC. Subsection CorynilH^sai' DC. 

L. and other Capj)aris species (Jar\ Is et al., 1993). 


Corymbose inflorescences. Repr(\setilali\"e species: C. 
Capparis comprisc^s around 230 s|)ecies (hstribuled in sqnaria L, C. umbeUala IJrown ex DC. C. incanesrcns 


ti-opieal and sul)lro[)ical zones of southern A 
Europe, Africa, Machi'i^asc'ar, Asia, Australia, and the 

Paeific Ishinds (Willis. 1988). 



f d 

le g(Muis, proN ided 

DC. subseclion Ociandrae DC. Idouers with 8 
stamens. Rei)resenlative sj)ecies: C. raccnndosa DC, 
C. olcuidcs Biuch.. C. coriacea Mnndi. 

New World taxa are includcHi in fi\e sections. 
Section 2. Capparidaslnun DC St 
thorny, oval s<^pals without gland, and short g) no- 
l)liore. I!e|)reseiitati\c ^pt^des: C. brasiliana DC. C. 
the first comprehensive niarroplivlla IIBK, C. nwea/a DC Section 3. 

ems trpnei'allv 

Candolh,^ (I8>2 I), who proposed a sectional di\ision 

s)slcmatic apju-oach to Capparis. OKI World taxa 
belong lo Section 1. Capparis (= Eucapparis DC). 
Representative specdes; C spinasa D. with four 
subs(^ctions. Subsection Capparis (^ Pediccllarcs 
DC). Flowers always solitaiA at leaf axils. In adiHlion 
C. spuiitsa and rtdaled s[teides, ollna- represenla- 


lives intdnde species smdi as C. 

('(frld(}ginra Decne. 

CynopJudIa \){]. Stems gencraH) thornv, o\a1 sej)a1s 
possessing basal gland or foveola, and lar<^e ^yno- 

phore. Hepresentativ(^ spec ies: C. cynnpludlopliora L., 
C guayaipdlaisis I IRK, C. anijdissinia Lam. Section 
4. Calaalhca DC Bounded fruit seelioiu thin sc|)Lds, 
bnear, and sharp, lieprcsentalive speides: C neaio- 
rosa Jae(j.. C pulchrrrinKr Jac(|. Sei-llon 5. Rrcjaias- 

Son.e sp(Hdes with g<'ndnat(^ Oowers or In buncdies of hum DC. Triangular sepals, sharj); always very short 
three, rartdy aioiK^ such as C. Iwrrida L f.. C. gynophore. Repres<mtati\ .- species: C. ferrui^inra L.. 

pidfiJJora DC, and C atnrscens D('., 



er C. Ificana IHRx. C. indira (L.) Rawc. & Rendle. work was part of die l>l,d). Dissertation prese.iled I,) C liu.eenc iu to the Facnllv of Hioloj^y, Mureia. Spaiti. We thank 

Ik- l()lluuMi^ luahnria ari(l their staff for pn)vi(ling lf)a]is. ae(-ess t<) (■()]l(vMi()iis. aiul a>M^lance- HISR |J.M \\\{ C j' C III 15 
WL K, JK. JKPS, LtV. MA. MARSSj, MLH. 0\F. P. K\C RSA, lAHI, and LS. We thank Pedro Pe rales A a drawing 


Fignre 1. Sp<>eial gratitude is due to Joelien M.iller (.IF). \ la.linin Dorofeev (T,F). S.MVfia Manua- (OXF). O.-nna Yonng (1 W) 
and^ Mjos Firjeii (K) [uv llieir help ,n finding type material. This ivseaud, ua.s snpporled hv a ^^rant fomi the Spanish \IinisUT 
ol I'.duealKni and Cidtnre and hy the projeel A(d'^<>()- KViO oC r){;i(:Vr. 

"Hie etiitors nJ the . l/;//f//.v tfiank Sophia P.alconil. for her edilnria! eonlriluition to lln> article. 

;M)epnrfamen]o d.^ Bi(.k.^,'a Vegetal, Facniiad d.- Biolo-fa. Fniversidad de Mnrca, IvI^OlOO Fspinardo. Mureia, Spain. 


'Depaitaincnio de I]iologia \plieada. Fs(iiela Pohu'cnica Sup(-rior de Orihncia, Fjiivrrsidad Mi^ 
Driluitda (Alicante), Spain. 

uel lleniande/. VAYXWl 

Km. Missouri Bot. Gai^d. 93: 122-149. PiiiEisiii:i) on 31 iVIx^ 2006. 

Volume 93, Number 1 

nocencio et al. 

Revision of Capparis Sect. Capparis 


SecLioii 6. Quadrella DC. Aii^ulaj- fruit section. 
Representative species: C, jdindiccfisls Jacq., C. 

inlcrmcdld IIBK, C. crotonoidcs IIBK. llie species 

Capparoideae are almost always fleshy in nature in 
contrast to the o]'len dry fruits of Clcomoideae and 
Brassicaeeae. Flora! synmietry, slaineu number, leaf 

C. di'cidiKi (Forssk,) Edgew. with deciduous leaves, up type, and fruit type all show homoplasy. Clades within 
to 20 X :5 mm in size, is included hy Candolle (1824) Ca[)[)aroideae show a l)iogeograplhcal i)altern based 

on this sampling with a New World (dade (all New 

in the genus Sodada Forssk. 

This was foUowed in part hy fh'utham t^ 14ooker WorkJ re|)resentatives of Capparis, Bclcncila Karst., 
(1862), although ihey created three new sections: Morisonia F., Boscia Lam., and Cadaba Forssk.) and 

section Sodada (Forssk.) Benth. & Monk, including C. 
decidaa; section Bushcckea (FndL) Benth. & Hook. 

an Old W'orUl clade {Maeriia Forssk., Tylachiiim 
Four.. Ritchica R. Br., and Cadaba). The Old ^'orld 

inchuhng Australian species; and section Beauleinp- sp(Mdes Capparis lomentosa Lam. is nested within an 
sia (Cau(L) Benth. & Hook, including one American otlierwise New World clade (l)ased only on //7/F-//7^F). 

Oh I World Capparis spinosa, the type of genus 

Capparis, is nested within an Australasian (dade, with 

ApophyUiiui anomaluni F. Muell. (westcjii New South 

I Vi^'st Asia. He Wales) and Capparis callophyUa Blume (Java) (based 


Zohary (1960) proposed new systemalies based on 
a [)artial geographical review- of this geiuis restricted 
to the M(Mliterranean region an( 

recognized two biogeographical groups: the tropical, 
in(duding Capparis decidua, C. cariila^inea, C. 

onlv on //7/L-//7^F). 

DNA sequencing of the 

chlun)[)last rchl. gene 


n. inclu(hng nested New World Capparis hasiala jacq. and Old 

sj)ecies that have lost their links with ifie tropical 

World C. saadnirhiaua DC. in the same clade, but 

African stock (C. spinosa, C. sinda VedL, C. sampling was restricted to these two CV//v>r/m species 
Icucujdiylla DC). All species belong to section and comparison was made with Crafacra L. species 

Capparis in the sense of Candolle (1821). 

Jac(»bs (1065) attended to the Capparis species from 

(Rodman et al., 1998; Cummings et ah, 2003). 

Taxonomie confusion of Capparis sect. Cappans is 

India to th(^ Pacific, and organized them into four reflected In the number of combinations and changes 
sections: 1. section Capparis, monotypic with C. of rank, with frequent placement under C. spinosa 
spmosa, sJ.; 2. section Sodada, monotypic with C. (Zohary, 1900; Jacobs, 1965: Higton & Aken)yd, 
deridua; 3. section Mouosticharalyx Radlk., in a new 1991). Capparis spinosa has become a blanket 

identification used to cover the scarce level of 
definition of the taxa in Capparis sect. Capparis 

f tl 

le species 

eircunrseription containing most o 

formerly included in section Capparis (— Eucapparis 

DC), with about 65 species in the area under revision; (Greuler el al., 1984). This has both taxonomie and 

4. section BusJw.ckea, with 14 species in all. 

lligton and Akeroyd (1991) reviewed ihe diversit) 

economic impHcations, as Capparis [h>wer buds are 
the crude material used as commendal capers and 
<)fG/yv^am in die Mediterranean n^gi(Hi, especially in variability in this economic pnxhict is determined 
connection with C, spinosa, examining six species in mostly by taxonomie differences (Inocencio, 2001; 

Inoceneio et ah, 2002). Molecular studies of Capparis 
sect. Caj>paris have been scarce or restricted to small 

one section, which Avere finally nMlnced to a single 
species with two sulispeeies. 

Hall et al. (2002) analyzed scipumce variation for sampling (Fici, 2001). 

a large sam(>ling of Brassicaeeae and Caj)paraceae, 
using two chloroplast regions, /r//L-/r//F and ndh\\ 

A genetic fingerprinting technique (AFLP) was 
used by Inocencio et al. (2005) to examine the 
Idu; results of parsimony and likelihood analyses relationships among Capparis species. Genetic dis- 
strongly supported the mono[»hyly of Brassicaeeae 
plus Capparaceae and recognized tliree clades: 

tanees, based on AFLP data, were estimated for 45 
ac^cessions of Capparis species from Spain, Moroc("o, 

Cai>[>araceae subfamily Capparoideae, subfamily and Syria. The results of this analysis sup])ort the 

Cleomoideae, and Brassicaeeae. Habit an 

d fruit differentiation of four (C. oricnialis Veilh, C. sicula, C. 

characteristics demarcate tlu^se three clades. All aegyplia Lam., and C. orala Desk) ol the live taxa 
Cafiparoldeae are woody, which is the plesiomorphic sampled. The fifth, excluded, species was C. spinosa. 




for the Brassicacccie aud Caj)[>araceae 

The grouj) of plants recognized as C. sj)inosa on the 
basis of moqihological characters such as shrub 

clades. The herbaceous habit i- gtMierally found in 

Cleomoideae and Brassicacea(;. Indt^hlscent, fleshy procumbent or somewhat erect, stipules nsnally weak 

fruits arc plesiomorphic in Capparaceae and Brassi- or vesllgial, raridy strong, very long and thin (0.3- 

caceae and are the dominanl frull type of Cappa- 0.6 cm long), Indument on leaves always very lax, and 

roldcae. Brassicaeeae and Cleomoideae both have 

dehiscent capsules with a replum, a synapomorph) 

tritdiomes thick and long (300-500 [i\u h»ng), is h>und 

almost exchisivcl) in cultivation. Several cultivars of 

shared bv these two clades. Tiie dehiscent fruits of C. .s7;///asv/ appear In an intermediate position between 


Annals of the 

Missouri Botanical Garden 

C. orirnlalis and C. sicula am! (ncrlap with C. C. pumflora, C. sirula). The S.i(hmf)-/anih(vian 
ortcnlalis. Vlw olhcc Iwo species, C (icgxpiia and (1. R 

r'gl(Mi (Paleotvopical) is inliahiled hy three species 

o/Y//^/, are morplinlogieally (hstinet, eharaclerized by in tropical lui^t Africa, httural Arabia, uesterd India 

ihclr hahit, stiptdes, and h'a\(\s (C. aegyplin: >Iirul)s and sotidierii Pakislan (C. wurrmnfolia, C. luinijlora, 

soincwhal erect; (wigs gray-gnHMi or hlne-green wilh C. sicula). The African Kanx.-Xanub and Indian 

waxy rnwr; siipnh's cur\ ed, relrorse; leaxes obovati! regions are inhabiled by one singh^ species each [C. 
to o\ate. bases and aj)ices loundtMl. 2-3 X 1.8-3 


hercrornsis and C. sicida, n\specti\ ely). Capparis 
C. orafn: shnd) [ienduh)ns; adult leaves oval(% sicula is Hk; most widespread species, strelching from 
lexUnv sul)C(>riaceons; sllpides curved, mostly an- ihe W(vslerM Medil(MTancan lo die I [imalavan Moun- 


tains and die Rajaslhan of India (Indii 




llie objecti\(; of the present revision is to [)n)\ ide Paleotropical). Capparis heveroensis, \n weslern Na- 
a general taxonomy, based finidamentany on morplio- iiiibia, is the only species confined to die African 

logical data lor Capparis sect. Capparis. 

T.woxoMu. C().\ri-Ar oi <7i/vmavs skct. C.\rr\i{is 

Karoo-Naiiiil) Region (seiisu Takhlajan, M)o()). En- 
demic laxa are infre(|ncnl in ihi,-. section, although C. 
aflanlica is endemic lo the Atlas ranire in ^h)^occo, C. 

mucronijoha Roiss. subsp. rosanoriaua (R. l''cdlsch.) 
Capparis b<d(>ngs to the snbfainily Capparoideae Inocencio, D. Rivera, Obdn & Ah'araz is (aidemic to 
(Capparaceae). that also inclndes Cadaha. Crafarra, central Tajikistan, and C. parriflara Roiss. subsj). 
Marisoni(K Bascia. and odier .\e\v World and (Jhi -Vj//r;cror^//7>a Inoccaicio, D. Ri\ era. Obon l^ Mcarazis 
World genera (Mall (4 ah, 2002). The difleriail genera endemic ((. the western provinces (Ninini/, Farali. 
overlap in moh'(adar sludies (Hall el ah, 2002), 

Herat) in Afgliaiiislan. 



marked hi 

annougn a markcfi !)iogeogiaphical distinction is 
h)Lnul between New Vi'orld and OhI World ot(hi|)s 
reeogni/ed al die level of section or subsection 
(CandoHc, 1824; Ih-nlham cS. Hooker, 1862; Had 
et ah, 2002). A lentatixe inhag^Mieric 

Eco.NoMic l\M'(][rr\x(:r 

presented in d'abh- 1 in ortK'r to 
Capparis sect. Capparis. d'here are iTunn nnresolvr^l 
taxonomic and nomencialnral issues for infrastrncture 
in Capparis. Tlieivhjre taxa in d^ible 1 are merely 


pnxsented as a syndiesis of major gron[)s. 

S])ecies ol Capjxiris sect. Capparis are widtdy used 

livisi(m is as hxMJ and mechcinc in ihc Old \\\n-hh Capparis 

conlexlualiz(^ si)inus(i is almost ex(dnsi\ely kMo\vn in culli\alion. 

The supposed wild indivichials of C. spiuifsa are often 
remnants of anci<'iit caper fields or esca[)ed from 
cidti\alion. hocal cap(M' culti\ars and edmo\ariclies 

are recognized througliout tlu 

Gi'OcatAi'iiic DiSTimuTioN ami Exokvusm 

Mlg to C, 

Western and central 
Mediterranean region (Spain, Franc(*, Ttaly, continen- 
tal and insular), dliese principally heh 
spinosa. ])ut also to C. orientalis (Rivera et ah. 1999, 
Caf)pans is mosd} a Pantropical genus, but section 2003b). I''Iow(m- buds, consumed as biined product, ai'e 
Capparis rs ahu(>st strictly Holarctic wilh six (exclusive a ricdi soui-ce of the antioxidani pluMiolic compound 
species {(L acgyplia, C. athmiica Inoceneio, I). 
Rivera, Obdn 0( Alcaraz, sj). iiov., C. oriciilalis, C. 

rutin (Inocencio et ah, 2000). The use of Capparis 
species h\ Immans lia> l.)eeri traced to the Prehistorv 

0}(tta, L. spiuosa, C. zahar)i Inocencio. 0. Rivera, and earl\ historic times of Western Enropt^ (lst-2]id 

Obdn cK' Alcaj-a/. sp. nov.), one paleot topical species eenl. A.I)., Tong(a-eM, Uelgium), the Medil 

(C. hrreroeusis Schinz), and three in liolaictic and 

paleot ro|)!cal aj-<^as (C. niucranijalia . C. parrijlara 


region (9()()()-7 100 R.C. Franchli Cave, (neeee). and 
\\est Asia (9th-r>lh mill. R.C, Tell Murexbit, Syria), 

Boiss., C. sicala). Here w^e name the florislic as evidenc<M! by the presence of these sjteclcs in 

calegories (kingdoms and regions) according to 

d\ikhtajan (19o0). Capparis sect. Capjuuis has its 

diversit)- in the i\l(Mhterranean Region 

(Hohu'ctic) with seven s|)ecies [C. aegyptia, C. 

adanlica. C. orirnlalis, C. oral a, C. spinosa, C. 

archaeoh)gical sites (l^ivera el ah, 2002). 

maximum di 

M \ti-:kiai. \xi) Mi^Ttinns 

The herbaria and libraries of die following irrstitu- 
zoharyi, C. sicula). \[ is followed next b\ the Saharo- tions were consulte(h RM, E, JEI\S, K, MA, MUR, 
Arabian Region (also Holarctic) with six species ni 0\F, \\ USA, and I. Mil. Specimen., on loan uere 
North Africa and the Arabian Peninsula [C. aegypiia, reeei\ed from RISIl, RR C. C. HER, IIUJ, MARSS.E 
C. orala, C. zoharyi C. niuintuijolia, C. parrijlara, C. 
sicula). The lu 

mo- 1 u rani an Region (Holarctic) is 

RN(i. and I'S. Special collection trips were eondncled 
in North Ahica, weslern y\sia. and Mediterranean 
inhabited by fom- speeies extending along most of Spain lo obtain fresh material for molecular studies, 
West and Central Asia {C. acgyplia, C. mucrnnijolia, for the in vivo study of floral charac^ters, and for 

Tabic 1. Tentati\L' iiifrageneric di\ isioii of Capjuiris prchctited in order lo rotilextualize Cappans seelion Capparis. 

Infrageneric rank 

Sect. Brcynitislntni (Plum.) DC 

Seel. Calfinthea DC. 

Seet. CapparlJastruni DC 

Seel. Capparis 

Seet, Corrmhosae (DC.) Span. (= Subseet. 
Curynibosde DC. Sect. Monostichocahx 
Ratilk, p.p.) 

Seet. Cv/iophalla DC. 


Branehes unarmed. Leaves large (more than 0.3 em wide) 
and [jersislent. Floucis In simple or eompuund 
iiiiloreseenees (raeemes. umbels, eoryniljs), ailhougli 
solitary flowers al llie leal axil ma\ ap|)ear in some 
indi\ iduals. Sepals triangular", sharp; ^) iiopliore alwa)'s 
very short. Flowers with numerous stamens 
(> 50). Fruil romuk^d in eross section. 

Lea\"es hirge (more than 0.3 etn wide) and persistent. 
Fh)^\■ers in simple t>r compound inflorescences 


(racemes, umbels, corymbs), althongh soHtary flowers 
al th(^ leaf axil may appf\u' in some in<h\ iduals. Sepals 
thin, linear, and poinUnL Flowers w^ith lumierons 
stamens (> 50). Fruit rounded in eross section, 
ems generally thorny. Flouers in simple or eompoimii 
infltireseenees (racemes, umljels, corymbs), although 
solitar) flowers at tlic leaf axil may apjicar in sijine 
intllviduals. Lcavt^s large (more than 0..3 etn uide) and 
persistent. Sepals oval without gland. Flowers uith 
numerous stamens (> 50). Gynophore short. Fruit 
rounded in eross seelion. 

Flowers always solitary at leaf axils. Plants with flowers 
sliglili)' zygomorphie, abaxial sepal not galcate or 
sliiihllv saleate. Flowers with numerous stamens 
(> 50). 

Brandies Luiarmcd. Fea\es large (more than 0..3 cm wide) 
and persistent. FUnvers in corymbose infliirescences. 
Sepals rounded; gynophore \ery short or large. Flowers 
with mnnerous stamens (> 50). Fi'uit rounded in cross 

Stems gtMierallv thorny. Mouers in simple or com[)ound 
inflorescences (racemes, umbels, corymbs), although 
solitary flowers at thi^ h^af axil may a])p<\u in some 
indi\iduals. Leaves larue (more tlian 0.^^ cm wide) and 
persistent. Sepals o\'ale [lossessing basal gland or 
foveo](\ Flowers w'itli numerous stamens (> 50). 
Gynophore large. Fruit rounded in cross section. 

Represenlati\"e species 

C. ferruginca L., C. inama IIBK. 
C. indica (L.) Rawc. & R<'ndle 

C. nemorosa Jacq.. C. pulchcrruiui Jacq. 

C. hrasiliana DC, C macrophyUd HBK, 
C, cuncata DC 

C. spinosd L. 

C. sepiaria L., C. umbellala brown ex D(^ 
C. incanesccfis DC 

C. cynophallophora L.. C. guajaquilensis TIBK, 
C. aniplissima Lam. 


New Woi 

■ ( 

New ?;^orld 

New \\"oi-ld 

Old \\()rld 

Old W OT 

* ( 

Ne^v World 






CD o 

< o 

in CD 





'I'aljle 1. Cunllnucd. 

liilratreneric rank 

Srcl. Giiledtdc InoceiU'iu el al. 

Sci't. Ouadi'vlid DC. 

Sfcl. Scridles (DC.) $])aii. (= Siilisrct. Serialt's 
DC. Ser-I. VlftnostirlifK-alyx H;nllk. p.p.) 

Srcl. Sodada (Forssk.) I5ciilh. tli Hook. 

Suhsect. OcUiifdrae DC. 

Siih-^cct. Pt'did'Hares DC (= Srct. 

Mouostichocdlyx Raillk. p.p.. Srcl. BusbecLia 
(IamW.) Bcnih. & I look. ]).p. 


I-'iowers always suliiarv at leaf axils. Piaiils with I'iovvers 
slroiiglv zygonioipliic. abaxial sepal stronglv galeate. 
Flo^vers w'llh numerous stanirns f> 50). 

Leaves kirge (more llian 0.3 cm wide) and persistent. 
FloAvers in simple or eompf>nnd iniloreseences 
(raeenio-. umljels, eor\nil)s). although s()litar\ flowers 
at the leal axd ma} appear in some indi\i(luals. 
Flowers wllli numerous stamens (> SO). Fruit an^rular 
in cross stn'tion. 

I^ranehes iniarrned. Ft^aves large (mure llian 0.3 em wide 
and peisislent. Infh>r(^sct?nees racemose oi' in series on 
the stems. Sepals roimded. Flowers with numerous 
stamens (> 50). G)nop]iore \ei"y shorl or large. Fruit 
rounded in eruss seelion. 

Leaves thin. 0..3-2.(l X 0.1-0.3 em. (leci(hious- FIowim's in 
simpk,' or compound iuflorescences (racemes, umlxds. 
eorvmbs), althou'!;li solitary (lowers at the leaf axil mav 
appear in some indi\iduals. Flo^vej-s wilh numerous 
stamens (8-18). 

Branches nn;irfned. Leaves large (more than 0.3 cm wide) 
and persistent. FIttwers in simple oi' compound 
iiinnroscenees (racemes, umhcls. cor\m[.)s), allliough 
solitary flowers at the leaf axil may appear in .-ome 
indi\iduals. Sepals roundetk Flowers wilh 8 stamens. 
Cvnophore veiT shojt or lar^e. Fruit rounded in i-ross 

Firauches unarme(L Flowers geminate or in hunches of 
three. I'arely alone. Leaves lai'ge (more than 0.3 cm 
wide) and persistent. Sepal > rounded. Flowtn's with 
numerous stamens (> 50). (iMiophore very short or 
large. Fruil lounded in cross section. 

Repri's<'ntati\e species 

C. carlilagined l)e(uie. 

C. janidiccnsis iacq.^ C. intermedia IIBK, 

C crotonoidcs HBK 

C. zcylanica L, C. acumiiuila V( illd., 

C, (/uddrijlord DC, C. rotundifolia Rtjlll 
C, hreii spina DC. 

C (lecidua (Forssk.) F.d<:ew. 

C. raccmidosd DC. C. dleaides Burcli., 
(J. coriaccci Bureh. 

C, liijrnda L. (.. C. puhiJJora F3C, 
C ranescc/is DC 


Old World 

New \^^n-Id 

Old W m-ld 

Old W^orld 

Old Wuvld 

01.1 World 













Volume 93, Number 1 

Inocencio et al. 

Revision of Capparis Sect. Capparis 


Table 2. List of n 


ical characters c(tnsi(lcrcil in the sluilv. 


1. Phnit hahit 

3. Twig shape 



Twig cftior 

5. hilci-iu)(h's 

6. SiipLil<' shape 

7. Slijmle orientation 

8. Si 



9. Stipule color 

ID. hea( shap(; 

I 1 . Ilase ol the leaf 

12. Leaf apex 

L"^. Miicro pn^senee ami 

14. Miicro sha])e 

1 .1. Leaf textnre 

16. Leaf \eins prominence 

1 7. Pelinh- l<Mlglh 

18. Leaf ahaxiaJ uuhnncnl 

19. TiichuEiie thickness 




r f 1 

IVichotae length 

21. Fciiilc floral pedicel length 

22. I'ertilc floral pedicel ihlckness 
2.1. Klowei- hnd apex 

21. /MiaNial sepal 


ower svmnielry 

26. Nuniher of stamens 

27. Anllua- length 

28. \nlhfM- apex 

29. Irnil shape 

30. Pnlp color 

31. Seed color 

32. .Seed size 


Krecl / procumhenl / pcndulou.s 

Maximnm length of the stems in meters 

Torliiose / straight 

Green / yellowish / reddish / waxy 

Length in millimi'ters 

Cni\<'d / somewliat eur\r(l / straight / setaceous 

Spreading / retroi-se / anti'orse 

DecLirrenl / not deeurrent 

Orange-yelluw / oratige / golden-yellow 

Rounded / o\ale / lanceolate / ohlong / elii[)tical / ohcoidate /ohovate 

()hlus(;/ tapering / aciile/ eoitlalc 

Aenle / r-ounded / oijcor(hile / obtuse / truncate 

Long (1-1.5 mm) / small (0.5-1 mm) / very small (0.1-0.5 mm) / lacking 

Straight / cur\('d 

I lcrl)a<-enus / lleshv 

I^ronnncnt / not profmnent 

\rv\ short (less than 0.5 em) / short (0.5-1.5 cm) / hmg (exceeding 1.-) tin) 

Vci'y dense 

/ (](ms(^ / densf^ to lax / lax / very lax 

Thiik (25-50 pm) / diin (15-25 jim) 
Long (250-900 |.lm) / sho.-t (50-250 |am} (greater than 1 cm) / ^hort (1.5—4 cm) 

Thick (over 1 mm) / slcn<ler (It-.-^s than or e(]ua] to 1 itmi) 

Acute / rounded 

Calealc / >hghth galeale 

/\gomor|)hic / somewhat /ygomoi-phic 

Nmneions (100-150) / not so numerous (40-80) 

Very small (2 timi) / small (2-3 mm) / large (3 mm) 

Hounded / acule 

Hounded / ellipsoidal / ()!io\aI<' / ohlong 

Hed / \ello\\ 

Brow n/ da["k bi'ou n 

L<'ngth X width 

dcjtlli in millimeters 

[>rej>aring exsiccatae. Voitcher specimens were dc- Dislriluillon of species comprising several subspcclt's 

is represented in Figures 2, 4, and 5. Habitat is 

descrilxnl tising the available data on nernarium 


posited in MUB and UMIL 

Here we l:)ase species on morphological and 
biogeographical feattires. The species represented lal)els and those reported In ibe protologue of each 
are more or less distinct, hcLerogeneons, and variable taxa. Phenology data are restricted to the flowcring- 

morpho-[)l]ysiological entities, the origin of vvhi( h is fruiting period according to the herbarium specimen 

associated with a partictilar environment and artvi in laliels and tlie protologue. 

agreement with Vavilov (1931). Taxa are defined in 

stich a way thai it is f(dali\ely easy to determine the Taxonomic CHARACTERS IN Cl/'/MA7.S SI-XT. C\rr\KlS 
ascription of each specimen to either one or another. 

Tluu'efore, extremely large and \ariabb; spctdes were 

We have shown thai molecular, pliytocliemicab and 

avoid<Ml. Discontininlics, both geographical and in vivo dala are useful for luiderstanding patterns of 
tuor|>lio1ogical (see v(^stiltlre, slipides, leaves, inflo- variation and, as such, were considered for the 
rescences, flowers, and Irnits sections in ihis paper), popidalions presetit iti Spain, Morocco, Syria, and 


are gooo markers, 

een annnei 


lied to tlie eritire section. Therefore- we 

but hybridization and hybrid Lebanon (Inocencio, 2001; Inocencio el ab, 2000, 

swarnis have obscured the definition of sp(Hdes and 2002. 2()0o); however, these m(4hods have not yel 

sidispecies. b 

New taxa are represented iti Figures 3, 6-0. selected (diaracters generally availal)le in herbaritiin 

Geographic dislributions have been [dotled (^xclu- specimens (Talde 2). some oJ vvhi( h have been used 

sivcly using the informalion from herbaiium sheets. for the first lime in this sttidy. lor example, anlher lip 




- - <..c- 







^ J 

t _ 

.^ >^ 

rii!;iire 1. I'lant hahil: ^A. Krcct, e.g., Ciippans zohani. Drawn from jilioto taken in Llano del Beal, Murcia, Spain. 
Mallorca. Spain. — C. PenJuluu^. e.g.. C. oricntalis. Drawn frt>ni ]>lioto taken in Palrna do Mallorca. Spain. 

— U. i^tK-uinl)enl. e.g., C. spinosa. Drawn frotn [)h(it() lak<'n in l.luhf. 











Volume 93, Number 1 


nocencio et al. 

Revision of Capparis Sect. Capparis 



ape was rcrogm/cM 

1 as a useful etiaraeter for coryinhose or racemose iiidoicsceiices. Flower l)U(ls 

identifying living, herbariutn, and processed material 


have acute or rounded apices. Flowers are 

[nocencio et al.. 2002); once characteri/ed in fresh bisexual and more or less zygomorplnc. Four green 

material, it is relalivtdy easy to determine in sepals are always present, frt^e. concave, having a more 

herbarium specimens by re-hydrating die anthers or less galeale (helmet-shaped) abaxial sepal. Four 

and using a stereomicroscope. Ad the selected white or pink petals are always present, free, oval, 

eharacters were studied in mature specimens with frequenll} unequal. From 50 to numerous stamens, 

open (lowers and ripe fruit. The quanlilative char- Anthers are small to large (Tabic 2) widi a rounded or 

actcrs are expressed using SI metric units. 

I'l.AN'r HABIT I\ Cl/VMA'AS .>1-:CT. C.1/VMA75 

Capparis comprises small 

trees, shrubs, or geo- 

sharp apex; androphore absent. Nectaiy situated in 
tlie floral disk, between the insertion of the petals and 
sepals, triangular in form, apex directed toward the 
flower's interior. N(H:tai7 mor|)hology can be a highly 
valuable taxonomic resource, but only available in 

phytes. All species of section Capparis are erect, ^^.^^^j^ ^^j. .^(dl-preserved material (Inocencio el ah, 

procumbent, or pendulous shrubs (Fig. 1). Some (C. 
sicula) l)ehave as a true geophyte, with imdergronnd. 

2002). A gynophore is present, usually exceeding the 
stamens in length. The ovary is ellipsoid, situated at 

branched perennial stems and decaying annual aerial ^,^^ ^^^j ^^^ j,^^ gynophore, unilocular, with (2 to)i(to 
parts (geothamne, s(^nsu Bocquet & Aeschiman, 


10) placentas 


Plants glabrous or with simple trichomes as the 
indument. Trichome types and the densily of 
pubescence on \arIous parts of the plant are useful 
eharacters for identif>ing some Capparis speelt\s. 
However, high infraspecific variation is common in 
collections identified as C. sicula, for example. More 
consistent vestiture Is found on the abaxial part o( tlu 

FRUifs IX cAi'ruas sect. cAriWRis 


The fruil is an oblong, ovoiiL (dlipsoid, or globose 

in color with well-defined 




is green 

nerves, along w 

Inch dehiscence later 

occurs. Seeds are from one lo numerous, and are 
generally brown in color when mature, immersed in 
oddish or yellow pulp. Seed shape, color, and 

a re( 





been noted to be of limited 

leaves, where density, tinckness, and length of the taxonomic value (Rivera et al.. 2002). 

indument (Table 1) may be analy/.cd lor each taxon. 

Taxoxomic Tkkatmkxt 


Spiny stipules developing at the base of die petioles 
are absent in some species (e.g., Capparis oriralalis 
or are early shedding (e.g.. C. hcrerocnsis, C. oiala, C. 
spinosa). Stipule shape, eolor, direction of curvature 
and decurrenee at the base are distinctive characters 

(Table 1). 

Leaves are simple, not divided, alternate, witli 

petioles well difh'rentiated. Leaf moi-phology fur- 
nishes distinctive i-haracters (shape, texture, base 
type, apex type, presence and type of mucro) (Table 2). 
The size and. much less, the shape of the l(^a\ es are 
variable within many spet;ies. Leaf size es])ecially 
depends on water availal.>ilily and exposure to winds 
and sun during die growing season. Petioh: length, 
although variable within species, can be sorted into 
three groups (Table 2). 

Capparis L., Sp. pL: 503. 175:5. TYPE: Capparis 


The flowers are solitar) in the axil of the leaves. 
This is a distinctive character for the section. In other 
sections (except sect. Caleatae) the flowers form 



Beaulr/uf'sia Gaudicli., Voyage iioiiitc Bol. Atlas: lab. 56. 
1842 I 1 844^6]. TYPE; Beautcnipsid ariccnniaejolia 
Gaudicli., Voyage Bonito Rot. Atlas: tai). 56. 1812 

Hushnh'o ImhII., Prodr. Fl. Ins. Norf. 64. 1833. TYPE: 
Bushnkca nobilis Eiidl., Pntdr. Fl. Ins. Norf. 64. 18.33. 

Colivodvndmn Marl., Flora 22(1) (Belhl.): 25. 1839. TYPE: 
CuluiHlendnm yco Marl., Flora 22 (1) (Beihl.j: 2S. 

Dr.sHngi'sifi Gaudieli.. Voyage Roiiite Bot. Atlas: tah. 37. 
1842 11844-1840]. T^TE: Dcsfrugesia scubnda Gau- 
dicli.. \..yage Bonite Bol. Atlas: tah. 57. 1842 |1844- 


Homhak Adaus., Fani. 2: 402, 408. 1763. TYPE: Genus 
descrihed referring to Ei]>[)i MS. (Manuscript list of 
plants collorted in Ej^yi»l hy Lippi.) There arc no 
sprcirs associated with tile genus in the protolo^ue. 
However, the influreseenee tvpe, lack of leaves, and 
origin (Lipjii, hence Egy[)t) likely refer to Sodada 
dcciduii Forssk. {= Capparis aphyJUi Roth). 

Oligloron Raf., Sylva Telluriana: 109. 1838. TYPE: 
OHi^loron zeyUiuica Raf 

()lofu!ojnU\.. Sylva Tehuriaua: 108. 1838. TYPE: Olojulou 
racernosnm Raf 


Annals of the 

Missouri Botanical Garden 


sciidocroton Mill I. \i-<j;. 


2 1. 1872. TMM:: 

ora o.j; 
Psfiiil(frn)!ofi linclorius MiilL 
QuadrcUii (DC.) J. S. Pr.-sl, in Bmlil..hl ^ J. S. Trvsl.. 

Pnro/cnusli Roslllii 2: 260. MVl'^. TYPE: Qumhclla 
crotoDoides (Kuiilli) j. S. I'resl. (= Cappmis croloiundcs 
Kuiitli. Nov. Cm. Sp. S; 9n. 1821). 
.SoJ^/r/r/ I'orssk., ri. Ar<iA[)t.^ Arab: TM . 1775, TYFK: Sndada 
dccidua Forssk, 

Utcnrrui IJnioloni, PI. N(>v. Iloii. P>niM)n. 2: 8. 18:^9. TYPK: 
^ //en crid frondosa I i( ■ li ol . 

Cappari.s section Capparis TYPF^; lAij)jHiris spinosa P. g]j_ 

A lotal o( 10 species aiul 12 sul)s])ecies of ecdimiiile 
rclcvatice are reco^ni/cd. ilislril)Lite(l in the ln)|)ical. 


snhtropical. and Mcdit<'rranean /on(^s of both I 
splu^res. Widely j-cpre^etiled in Asia, and reaeliin 
soutliein Euroite, easlern, norlliern, and sonllnvestern 
Adica. A key for the species and reco*;ni/ed 
no[lios|)ecies cjf Cappaiis sect. C(ipp<n-!s is preseiiled 


Ky.\ TOTiiK Si'KciKsoK C \!'i'\i<is C\ri'{h'is\\ Asn, Imiioi-i:, 
amj Amjica 




very la.\). Mt'dilcrrantaii Eurjjk', WuiIi Altii-a. 
iMiddlr FasI inio India [Afghani si an, ADjania, 
Al<^t"i"ia, A/erhaijan, (A'prns, (Ii^orgia. rin^.'ce, 
India. Ifan. Irai]. Isiacl. Ilaly, Jordan. Ka/.akhslaii, 
Mongolia, Morocco. Pakislan. Sandi Arabia. 
Spain. Swia, Tuikcw Turkinniivian. Ukraine. 

Uzl>ckisian. Y 

9b. Shri 

procnmbcnt or sf)nic\\liat <'i'ccl; slipuli'S 
nsiially weak or- \('slif^ial. rarely stoni; indunient 

8. C. siada 

on Icayes always vcr\ lax. Medilci-rancan lMn'0|)e, 
Middle East in!o Tnrkc) fPrance, Greece. ItaK. 

Spain, Tuike}] 9. C. spinosa 

Flowers si i- Inly /) *^cHn(,)rpbtc; abaxial sepal 

1 1' 


sli<i;lilly galeale only lo 1.4 cm lon^, In 0.6 cni 


deep. Mi<ldle Fasl | ACghanislan, Iran, Ir^ 
Pakislan, Saudi Arabia. TnrknHMiislan 


7. C. parnflora 

Slipnl(\< inosd_\ anij-orse In orientation . 10 

SIniib |iendiilous; [nalurc leayes ovale; texture 
snbeoriaceous; slijailes curved. Norlb Africa 
(Alj^cria, Chad. Filna. Morocco. Tunisia 

P ^ 

6. C. (ff'dfn 

lOb. Sin lib <'recl: inatuic lea\es obJonj:; In n\)n\ ale: 
tcxlLire soniewhal coriaceous; slipules setaceous. 
South \bica [Nannbiaj A. C, hcn'rocfisLs 









PI a Ills una ruled, or w illi slipides \<'sligial or 
catlucous. Medilerranean Kui-ope and \orEli 
Africa | Albania. Algeria. Croatia. Greece. Italv. 

Fibya, Malla, Sf)ain, Turki^] .S. C. orii'nidlis 

Planis alua\s snin\ '? 

Stipuli^s relrorsc lo liori/ontallv orienled , . . . :\ 

Fi'nl lexlnre sonieulial fleshy 4 

Tui^s )t'llow or ^ra\-,Ln-een. not <ilaueous. wilhout 
waxy bloom; sli[)ules golden )ellow. not de- 

curreril. Middle Fasl [Afghanistan, Iran, Oman, 

Tapkishnu lYiiled Arab I'auirales 

4. C. miicronijolid 



igs green U) red-purple, or glaucous due lo 

a waxy covering; slipules orange, ikuauR'nt .S 

Sa. Sli]-nl»s erect; slipules slrongly dccauKail, Medi- 
terranean Furoi>e, North Africa, Middle Fasl into 
Turkey |Alg(!ria, Fgvpl. Greece, Israel. Joi-dan, 
Fcbanou. Morocco, Spain. S\ria. Turke\ | 

10. C ZohfllM 

Shrub [)rocumbcnt. or soiuewhat ei'cct or pendu- 
lous; slipules decnrri'ul lo nol d<'currenl 6 

Shrub pcntlulous; leaves lanccolah- lo o\ale- 
]anctH)lalt\ Norlh Africa [Algeria, Chad. Fil))a. 

Morocco. Tunisia] 6. C. orala 

Shi'ub proeumbeni or sonu^whal creel; leaves 
rounded or olutvalc to o\-ate 7 

7a. SI 

I rub pidcnmbeul; lv\rgs purplc-r-^-d; wilhout 
waxy bloom; leaves rounded, li[) acirlc. base 
rounded lo cordale. \nilli Africa [Morocc(d . . . 

2. C (Ultinliii} 

i 1>. Shnrbs sotuev\hat 

creel: tv\ igs grav -green 



8a. Fl 

glaucous, with waxv blootu; leaves obovate lo 
ovale, bases and apices rounded. Norlh Africa. 
Middle East into India [Egypt. India. Israel, 

Jordan. Saudi Arabia] PC. (ifgyplia 

Leaf lexliire herbaceous 8 

ov\cis zvgomorphic; abaxial >i'\)<\\ liehnel- 
shap(Ml, 1.7-2.3 cm long, 0.7-1.2 cm d<-ep ... 
Shnrh proeumbeni; stipules usually stoiil: pubes- 
cence on l<'avcs from lax to vcrv (k-use (rarely 


1. Cai>jKiris aegyplia Eani., Encycd. Method. Hot. I: 
60.), 1 i83. Capparis spinosa \ar. a('g\p>{i(i (Fani.) 

Roiss.. FF orient. I: 420. IP>67. TYPE: [Eg\pl] 

'Mapi a observe ce ('aprier en Egvple (v.s. in lierb 
Tsii.)"" (lectotype, designated beie, P-JL!: speci- 
in(Mi on sheet I 1.2 IP) right). 

Capparis sindifii VeilF. in Dnhamel, Traile ArTr. Arl)us|. |-M. 
2. Vol. I: 144. 1801. TYPE: It-gvpt] ■■|Iabilc. F'Arahie 
}>clr<'c, sur le MonI Sinai cl les mont agues ipii 
lY'uv ii-onneut. anpres dii village (\u Phai-agou. el siu' 


les chcniins enlre le Mont Sinai el le clialcau ou la \ ill 
dc Toi-. situes sur hi mer Pouge, oii il a etc ol)sei've par 
Beloiu IFuiwolf et Shav\" (lecl()ly|)c, I. 112 in Shaw, 
Cat. PI. Variis Air. I 7.'^ 8k designaled bv Pivei-a (M al. 
2O0:5a; ;i08-3()9). 

Capparis dcscrli (Zoliaiv) Tackh. lK' Poulos, Publ. Cairo 
Luivcr. Herb.. r>: 1 I. 1972 1197 IJ. Caj^paris spiiiusa F. 
var. ilcsvrli /ohary. Hull. Res. Coun. Israel 8D: 56. 
1960. TYPIv I Israel I Wadi Nosz. cnlr-aiu-e lo Wadi 
Fclnmu (Bir Dcdieba), 27 Mar. 1914. I\ IL Davis ,K: N. 

Frinhnin 5076-7 (lu.lnhpe. IICj!). 

Shnd) stjnievvliat creel, glabrous; Iwigs straight, uj) 
to 3 ni lung, gray or blue green due lo \ya\y cover lliat 
ap])ears ov(m- the entir<^ |)lant; inlcinoch's 1,5-1 cm: 
stipules curved, retrorse, slightly decurrent. orange, 
0.3-0. 4 em long. 0.1-0.2 cm wide al the base. Ft^aves 
ol)o\atc to (ivate, 2-3 X 1,8-3 cm. somewhat llc^sb); 
leaf veins nol promincnl; bases and a]nces rounded; 
tnucro ycvy small, 0.1-0.5 mm, straight or curved: 
petioles 0.5-1 cm. Flower buds rounded; floral 
l^edicids stout. 2.5-1 cm; (lowers slin-htly zv^onior- 
phic; abaxial (odtlj sepal slightly galtvitc al apex, 1.4- 
1.6 cm loug, 0.6-0.0 em deep; stamens 30 lo 80, 
anthers 1 .2-1 ,5 mtn, with rounded a|)ices. Fruit 

Volume 93, Number 1 

nocencio et al. 

Revision of Capparis Sect. Capparis 








Dislrihulloii map lor Capparis ovala (♦) (holli >ul).s|)ccic.s); Capparis spinosa (#); and Capparis aegyplia (^) 

Capparis (ic^)plia also occurs in India, beyond tiia]) ran^c. 

oblong, |)ul|) color unknown; ripe seeds dark brown. 
3.2-3.4 X 2.8-3 X 1.8-2 mm. 

lUu.sfran'nns. Plate 31(3) in Delile, 1812. Zoliary 

(1960: 32, ^i^^ 1). Tackholm. (1974: 163, pi. 48e)- 

Migalnd (1988: 48. pi. 26). 


Flowering and fruiting from (January) 

Maicli lo August (December). 

Dislribiifioii (ind liabilal. Saharo-Arabian, extend- 
ing into tbe Irano-Turanlan and Mediterranean 
Regions. Norib Africa, Middle East into India 
[Egypt, India, Israel, Jordan, Saudi Arabia]. Rocky 
places, steep sloj)es, al elevations from lo 2()()() m. 

often in 

Selected specimens examined. EC^4^'r. Cairo, Sclincin- 
furlh 995 (K); Gcbcl Ez Zebir. Sinai. Tadmor S-II7 (K); 
Abni^K LippL ? (P); Tadmor & Slimida S-120 (K); Sinai, Bore 
273 (K). INDIA. Maliablcsbam, Bombay. T. C. sji. (E). 
[SH VFF. Nabulus. Stail 266 (RN(;): Wadi Oclu Davis 4888 
(K); Fin (icdi, Lyschede s.n. (C); Kfar (VAvh and Manara, 
Curie 6S (K); Manara, Curie IKi (F); Mtjunl Cilboa, Daris 
4667 (E); Wadi Yarmuk, Davis 4604 [V). JOKUAN. Wadi 
iVlujib, Ma-daba. Boulos 5856 (K). SAUDI AHAJ31A. Wade 
Lahus, Jel)el, Collenette 7228 (K). 


* * 

le vicniilN of buman dwellings. It is tbe 

2. Capparis allanlica Inocencio, D. Rivera, Obon & 
Alearaz, sp. nov. TYPE: [Morocco] "Safi, 20-6- 
1999. Inocencio 60026''' (bob)l>[)e, UMII!; iso- 
types, MO!, K!, E!, MA!). Figure 3. 

SnfTrulcx decumbcns, usque ad 60 cm. eaulibus purpure- 
is, lobis rolundis. apice aculls, base roluntlalis, 1.5-3 cm 
lot)gis, 1 .2-2.5 em talis, a C. zoharyi differ!; stipulis 
lenni()ril)us, apieibus foliorum aeulis tiunqnam rolnmbs nee 
eordatis a C zoharyi el C. aegypfia diflcrt. 

Sbrub procumbent, np to 60 cm blgh, glabrous; 

common ca[)er in Egy[)l and is often associated wilh 
ibe IhjHUi'licnid hirta (L.) Stapf communily. Figin-e 2. 
Tbe type s])ecimen of Capparis aegyptia bas one 
flower, no fruits, h is part of tbe berbarium A. T. 
Danty tflsnard, wliicb is cited by Lamarck (1783): 
"v(i(bl) s(iecam) in berb(ario) Isn(ard)." It was 

ijicluded in 1857 in tbe Jussi('U berbarium (P-JU). Iwigs slraigbt, up to 
The specinum was collected "en face de Minia" in 
Egypt by one botanist who gave il to Isnard: *"l)oni per retrorse, slightly decurrenl, orange, 0.3-0.6 em long, 
tu" [Gift for you]. It was. presumal)ly, D. Lippi (1678- 0.2-0.3 cm wide at the base;. Leaves rounded, 1.5-3 
1704) himself. Isnard wrote the manuscript list of X L2-2.5 cm, somewhat fleshy; leaf veins not 
plants — now at P-JU — collected bv Lij^pi in Egyj)l prominent; bases rounded to cordate, apices acute; 
during liis last trip in 1 70 f (Pritzel, 1872). 

2 m long, redd i si 

1 purple, 

sometimes green; intejriodes 1-3 cm; slipules curved, 

nuicro very small, 0.1-0.5 mm, straight; petioles 
The basionym ol' Capparis deserti (Zohary) Jackb. & short, 0.3-1 cm. Flower buds rounded; (loral pedicels 
Boulos, Capparis spinosn L. \'ar. rleserli Zobar), was slender, shoi1, 2-3 cm; flowers sligblly zygomorphic; 
validly [)ublished by Zoliar) . However he states 'This abaxial (oild) sepal slightly galeale, l.t-L6 cm long, 
is a 'weak' variety because small-leaved forms occur 0.5-0.6 cm deep; stamens 30 to 80, anthers veiy 
almost in all grouj")s. 


small, 1.8-2 mm, apices rounded. Fjuit oblong, pulp 


Annals of the 

Missouri Botanical Garden 



J.A 9c 'CN 



2 cm 

10 cm 

Ft^jjUrr 3. Pctails ol [\u: iiru .spcclr.s Cappmis ntlanlica Itiocnuio. D. liivt-ra. ()1h')ii & V. Mcaraz. — A. Stem ami llitwci 
H. Di-lail of l(Mr (A, H draun U J. -A. Bam-fui fn.iu Jmn-.etuln 70100, UMII.) 

color uiikiiouii; n\)r seeds l.)rouii. 2.4-2,6 X 2.2-2.4 elevalioiis from lo 2()()() in., often in the \iei!nl\ (if 

X 1.6-1.8 mnu 



iiintan dwelliii^^s. In llie ^lurroundin^s of Moulay 

Phenology. V 

o w ( M" J n g and ( i • n 1 1 i n g f r o n i 


Dislrihulio/i and hablUiL Mediterranean I 

Rralniii (Moroeeo), it grows on clayey slopes alon 
May to wiih Ephedra K. sp., Tcucninn fnitianis [.., Laraiuluh; 

L. sp.. Clidfudfiops luinn'lls (J. C. ArchibdIiL 4.386. K). 


Norlli Africa [MonK-eoJ. It is I he coiiiinon caper 

FIgnre 4. 

Cappans ailanlica is a piocutnluMit shrub widi 

species in llie High Alias Moinitains of Moi-occo. pnrplc-red twigs: C. aegvplla is sonicwhal erect wilh 
Kound in rocky places, slopes, on calcareous suhslrata gra} -green or glaucous twigs; and C. zoIkuyi is erect. 
r marls, occasional on niclauiorphic snhstiata; at Hie stijjulcs arc not so slrongl) decanrent in C. 


Volume 93, Number 1 


Inocencio et al. 

Revision of Capparis Sect. Capparis 



Kigiire 4. Dislrilmlion map for Cupjxiris atUiniira (♦): (Aipparis orienlalis (•): and Capjxirls zoharyi (♦). 

ailanlica as !n C. zoharyi: the leaf tips of C. alhintini 

Dislrihiilion and habilal 

Karoo-Namil) ru^^iun. 

are r()unrie{ 


are acute, while lli(»>e of C. acgyplia and C. zoharyi South Africa [Nami1)ia]. Dune-forming sandy 

su])sLraLe, In coastal zones; al elevations from to 

100 m. 

The Sehinz herbarium is at /. At Z there are hvo 
sheets wilh tvpe material of Capparis licrrrocn.sis 

x'cause hololype is not designated in the prololo<;ue. 

raralypes. MOIIOCCO. Asni, Inmrnno 6()(}f)5 (IMIf): 
lall^ of Ou/oLi(l, Jury HTM (RNC); Marrakrch. Jury H7H:i 
(KNG): Moiilay l^-nliim. Arcluhuld }.mH6 (K): Quod Ai-a<.iil. 
Innivjino 6(}()():i (I'M III; Siksoua. f/fcatiT Adas. Hooker sjl 

(K): TafraoLitc, A./i. /6.^M'UNG); Tizi n'\v:^[, lnocenci(} OOd'i 1 y||^ speeiuKMi accompanied l>\ a single liaiidw rilnig 

on the sheet widi the following text, ^'Capparis 


3. Capparis lierer*M'Usi8 Sehinz. Ikdl. Herh. Bois- 
sier 1(3): :V)h. 1895. TYPK: [Southwest Africa = 

hererornsis Sehinz/Wortel, Walfischbai/1886/2 Bo- 

gen/N 1006/' is here designat(Ml as the leclotype; 


le specunen on the oiner 


iher she(i. with identical Sehinz 

Namihial "Sudwestafrika: Zwisehen Vi'ortid utid collection luimher, is a parah-ctotype. 

Walfischhai- October 1886, Scliuiz 1006" (lec- 
totype, designat{Hl here, Z!). 

Seh'cled sped mens excauined. 
\\>^^n. Saluorks, Ward 92S0 (K); 

NAMIP)IA. Walvis Ray 

I ler(M"<iland. W alfisclihai, 

ci 1 .1 .11 . ' .v.^.a,t .... o. Sehinz 1006 (/); Conception Hut. Ward iK: Ward 15^ (K). 

Shrul> erect, ahtiost glabrous; Iwigs straiglit, up to v ^ t 

3 m long, yellowish green; iutcrnoiles 1.3-2.0 cm; 

stijjules autrctrse. mostly setaceous, not decurreuL 4_ Cap[Kiris nincroiiifolia Uoiss., Diagn. PI. Ori- 
ent., Ser. I, Vol. I: 3. 1843. Capparis .sj}in(Ksa L. 
var. fuucronifolia (Boiss.) Hedge & Lamond, Fl. 

sometimes falling or wxak, yeiiow 

How, 0.2-0.3 cm long. 

()J)5_(),1 (^ni wide at the base. Leaves oblong-obovate, 
2.3-4.2 X 1-1 .6 cm, somewhat fleshy, yellowish 

])ases tapering to 


green; leai veins promuient; 

Ir. lloch. Umr. Geb.: 7. 1970. TYPK: [Iran or 
Oman] "I lab. in Persia Australi et Regno 
Mascaiensi, Aiudier dl89...'' (leetotype, desig- 

rounded, apices rounded to somewhal truncate; macro 
small 0.5-1.0 mm, straight; petioles 0.3-1 cm. Flow- 
er buds rounded: floral pedicels thick and shoi-l. 2.3- 

4.5 em; flow(M-s slightly zygomor[)hic; abaxial (odd) Kkytothi: Sl ii>i'rcii;s or C\rr\!!is \nciio\U'()Li\ imiik Midih.k 

naU^I here, (^.). 

sepal slightly galeate, 1.6-1.8 cm long, 0.6-0.8 cm 
de<^p; stamens 30 to 80. anthers 2.5-.3 mm, uilh acute 
apices. Fruit clli[)soidal, pulp color unknown; ri[)e 
seeds dark broun, 3.8-4 X 3.6-3.8 X 2.7-3 mm. 

Phenology. Flowering from jauuary to April. 

East am) Cknumi, Asi\ 




Twigs sliglitl) toilLn>=.e; .slii)u!cs curved, retrorse; 
lea\es ovale, piil)esceuce \"(M'y la\; ^o^ver buds acute 

at apex a. 6\ mueroniJoUa suhsp. nuuronijolia 

Twigs siraiglil; stipules alitiosl slraighl or some- 
whal curved, retrorse (^r ofu^u spicadiu^^; leaves 


Annals of the 

Missouri Botanical Garden 



r ■ I ■ 1 



... * • * 

^^* ^^ ^^S 

I T r 4 1 V ■ 





-. ■' 

b * b . -, . . ■ 

1 1 k J . .' 


Fi<i,Lirr o. 

Dislrihulioii iiKip foi" CdpjHU'is pdrnjloni ( ^lO (llin-c siihsprtirs): Cappuris siciiln 
('iipiHuis iiiiicronifolii} (^) (Ih)IIi sLil)s|H'(.'ics). 

all li\ (■ >it!)>jH'ci('.s); am 

olilniio^-laiK-coIatr. jnihrsccncc la\; flower hikls 

Uniled Aral) Kiiiiralcs]. Rocky 




ra\ UK'S aiK 

•^ ' sloiiy plains ol (icscrls, wadics in Aiucia scyul Uv\, 


Figure 5. 

la. Capjuiris iinicroiiifolia Huiss. snbsp, iiumto- 




(ipjxiris ellipdcd [lausskti. & U(fiiiin. ex Roriini. \ai-. 
niasLafrnsis ihiiisskn. tK R(a-taii. r\ Borniii.. Mill. Tluir. 

Iiafiifuada. at clpNations fiDm lo lOOO iii. 

Ilirre is no (l('>i<i,iiati()ii of holdlvpe Un Capparis 
iniicrouijniid liy Roissier; tlir lyjx- nuUcrial c'dcd 
cuniprir^t's dilfereiil ^[)r(.'inirM> t'ollcflcd I)) P. \[. I!. 
Au('lu;i- l'd(»y in son (hern Tcan and Oman 



kingdom of Mn^ral), widi collt'c-lioii luimlxas 4189, 

Hoi. Vrr. N.F. M: 19. 1891.. n VK: [ihuiu:] "(olii 
laliuiiljus ovalis; in iii[}il)(i> ad Maskat. |,/. Boruniidlcf 
ex. 46'' (k'fU)[_\pe, ilcsi^iiiatcd lu-ie. jF!). 


MOO. and 1192. dnrliig Ins (ra\t'ls in \?;X. 


Slnuh soiiU'v\lial erert, liea\il\ I.ranclicd. inc^ii- P^^^'^^ inncn)n!juli(f I Roissi 

TluMeforc l('('tol\pil'lcali(Mi is iieodrd. Tlio slu'cl with 
ihr It'tloI\ |)c c'onlains llie Inllou iti<^- hihels: [ ''Cap- 

. II ''An(in'r-Eln\- 


larly and uidcl) sprtNuling. up lo I 

llrrhier (rOiieiil N". 4189." Paialv[K's aiv Anrlicj 

laiiy anil uiiicix sprtNunng. up In I ni high; Uvn-s 'i^'-^vi viwu^m i-* . -t±(.jy. iaiui\[H*s mr ;\ni-i 
slightl) lorlnose, approximately 2 m long, ye[lo\\i>h oi- I*'- '^^^- ''■'^^** ^""' ll^-^S. (,[, lso1eclo_\ pes aic In K! 

grayish green; Inlernodcs O.r)-',] cm; stij)nlcs (air\cd, 
retrorse. uol d(MairrenF gold(Mi u'llow. apc\ orange, 

C(ipj)(U-is clliplica llausskn. & lionim. ex lionim. 

Milt. Tluii. Rot. \rv. N.F. VI: 49. 1894. is a laler 

somellmes pnhescenU al least hasallv. 0.2-0.() (an '^f>inon)nt ol Cupparis ellipltca Sf^an. e\ F. Muell. 
long. 0.1-0.2 cm wide al die base. Leaves ovate. 2-1 ^^' 

la Fl 

agmenia i'n\ lographiae Aushallae 9; 172. 18/S; il 

X 0.5-1.5 cm. .^onle\^hal (lehhy; Indnment \er\ lax. '"^ wilhin the range of Cappavis nmcwnifolia suhsp. 

triehomes thick and shorl to Ion*!. (20i:iO-l() X 200- 

O X / 

dOO pm; leal veins no! prominenL; l)as(^s usnally 



There is no designation (d" holol\pe foi' Capparis 
i'lliplicii \AV niiisluitrnsis llaiir^skn. <.■< Rornni.: the t\pe 
malerial la'led com|)rises (hHtavnt specimens eolh'ct- 
0.4 cm. l-lower hnds a(ail(- floral pedic(ds slender, ^*^^ under nntiihcr 16, by J. Ronmuilita- in his ^4ter 

lonnded, somellmes tapering, apices acnic: 
sinalF 0.5-1.0 mm^ straight; petioles \(a-y short, 0.2 

sliort. 2.5-8.5 cm; flowers 



ahaxial (odd) sepal sllghllv galcate, 1.4-1.6 cm hmg. 

l\-rslco-turelcnm 1892-1805/' I laussknechl's lier- 
harinm Is al .jF; Rorminillcr worked from 1004 as 

O.i-O.O cm deej): stamens 30 to 80, audiers 1.:^- curator in JF, l)nt sold his lua-harium to R. Most of die 

1.5 mm, with round apices. Fruit oldong. pnl|) color 

Rornmuller Capparidaeeae material at R was de- 

uuknown; ripe seeds brown, 2.4-2.8 X F6-2 X 1.6- ^O-oyed during the Second World War. One Capparis 
1.8 mm. s[)ecimen with collection nnml)er 16 is al JE (j. 


Midlei-. jirrs. comm.j. Tlierefore lectotyplliealion is 
ne(^ded and [)ossil)l(\ The sheet wilh llie l<H:lolyp(; 
contains the following hdxds: I 'Tsotvpus/ Capparis 




Flowering from March lo Sep[cmb(a-. 

Distrihuiion and hal)itaL Sudano-Zamlx^zian and 
Saharo- Arabian, extend in <i; to the Trano-Turaiilan 

clliplira Hausskn. & Rornm./ 

\ar. mas 



Regions. Middle East [ Afghatnstan, Iran, Oman, (lausskn. .^ Rornm." II "j. RornnuilhM: Iter Persico- 

Volume 93, Number 1 

Inocencio et al. 

Revision of Capparis Sect. Capparis 


turcicLini/ 1982-93/ No 46/ Capparis spinosa L. v./ <)})1()ng-lanceolate, wilh marked longitudinal nerves 
Mashiiensis Hsk. & Bornm./ delerm.:/ Arabia aus- (Fedtschenko & Fedlschenko, 1906). 
tralis: in saxosis ad Maskat/ 1893. 25-5 legit: J. 

There is no designation of hololype by B. 
Fedtschenko; the type materials cited are different 
specimens collected by E. A. von Kegel \n south- 

Selected specimens examined, AFGHANISTAN. Griflilh, rp --i • . /r o i i • ^ i '..^ u:^ 

.^..Jn.. To^M o. T I. n...„v.e. /..£./ ; n ^vestern Tajikistan (former Bukhara region) dunng his 

travels in 1883. Therefore lectotypifieation is needed. 
Two sheets have been found by Vladimir Dorofeev in 
T .F containing type materi al . The sheet av i th the 
lectotype contains the following label: 1 "A. Kegel, 
Iter Turkestanicum/ In decliv. Orient, montium 
Aryktau [am ostlichen Abhange der Berge Aryktau]/ 
4b. Capparis mucronifolia Boiss. subsp. rosanovi- ^^^p,..^ Iloranty [hoher als Goranty] 1200-20007 3-15/ 

(B. Fedtsch.) Inocencio, D. Rivera, Obon & yiyy 1883." The sheet with the paralectolype 


Lemann 374 (K). tKAN. Baiij^ar Lang(;h, Davis & Bokhari, D. 
56176 (E); Chahhahar, Baluchistan, Runcmar 22417 (F); 
Zahedan, Gray-Wilson & Hewer 263 (K); Horniuz, / 
Bornmiiiler 5 (K). OMAN. Islal, Wadi Hani Kharus, 
Radclifje-Smith 4045 (K); Ruwi near Muscat, Miller 6003 
(E). UNITED ARAB EMIRATES. Halla, IDu])ai, Western 267 
(E); Fujairah, Liunley 38 (K). 


Alcaraz, coml>. et stat. nov. Basionym: Capparis 
rosanoviana B. Fedtsch., Beih. Bot. Centralbl. 

contains the labels: I ^'August 1883/ 14/ 
strecken zwischen Kurgantiife/ und Lechman, 1200 

2{)\297A9()6, Capparis rosanoviana\i.Vi^i\\^v\\., 13007 (links Wachschufer)." II "A. Kegel Iter 
Consp. Fl. Turk. Vol.11: 98. 1909. TYPE: Turkestanicum/ Sandstrecken zwischen Kur-/ gantiife 

und Lechman 1200^13007 (links Wachschufer)" 

[Tajikistan] ''Ost-Buchara: am ostlichen Ab- 
hange der Berge Aiyktau, hoher als Goranty, 
auf Felsen, 1900-2000', am 3. [= 15.] April 
1883 (.4. RegeV.)r (lectotype, designated here, 


Shrub sonieAvhat erect, well branched from base, 
irregularly and widely spreading, up to 1 ni high; 
twigs straight, erect or decumbent, up to 2 m long, 
yellowish or grayish green; internodes 1-2 cm; 

stipules almost straight or somewhat curved, retrorse, 
often spreading, not decurrent, yellow-goKlcn, 0.2- 
0.4 cm lonfi;, 0.1-0.2 cm wide at die base. Leaves 


Seleded specimens examined. TAlIlvISTAN. Kadajian, 

s.iL 277 (E): h(Hween Kurgan Tyube and Lechman, Regel s.n. 
(LE); eastern sloj)es of An'klau mountain, Regel s,n. (LE). 


1.5-2 X 0.4-2 em, some\^ 


fleshy; indument very lax, trichomes thick and 
long, 20-30 X 200-400 |ini; leaf veins not prominent; 
base usually rounded, apices acute; niucro long, 1- 
1.5 mm, straight; petioles veiy short, 0.1-0.3 cm. 
Flower buds rounded; usually with indument at least 
at die base; floral pedicels slender, shoil, 2-3 cm; 
flower shape unknown. Fruit unknown; ripe seeds 

Illustrations. Bobrov (1939: 7, tab. 1, fig. 2; 1970: 

8, tab. 1, fig. 2). 

Phenology. Flowering and fruiting from July to 
August (Bobrov 1939: 3; 1970: 5). 

Dislrihution and habitat. Irano-Turanian Region. 
Middle East [TajikistanJ. At the eastern slope of the 

5. Capparis orieiitalis Veil!., in Duhamel, Traite 
Arbr. Arbust. ed. 2, 1: 142. 1801. Capparis 
spinosa L. subsp. orientalis (Veill.) Jafri, Flora of 
Libya, Vol. XII: 3. 1977. TYPE: "-Capparis non 
spinosa fructu uiajore C. Bauh. Pin. 480. . . " 
(lectotype, designated by Rivera et al. (2006), the 
image in J. Bauhin, J. Cherler & D. Chabrey, 
Hist. Plant. Vol. 11: 63. 1651!; epitype, desig- 
nated by Rivera et al. (2006), [Greece] Sokastro, 
Dod(x;anese, Th. Raus 8382, E!). 

Capparis riipeslris Sm., El. Graec. Prodr. Vol. I: 355. 1809. 
Capparis spinosa L. subsp. rupesiris (Sin.) Nyman, 
Consp. Fl. Eur.: 68. 1878. C. spinosa L. vai\ rnpeslris 
(Sm.) Hook. f. & Thoms., in Hook, f., FL Ctlt. India 
Vol. I: 173. 1H72. TYPE: [Greece, Cn^leJ ^4n Cicla et 
Anllparo insulis, ad rupes" (lectotype, designated here, 


Shrub pendulous or decumbent, sometimes reach- 
ing great dimensions in shaded sites, glabrous; tw^igs 
straight, dark green, sometimes reaching more than 
3 ni long; internodes 2-7 cm; plants unarmed, 

mountains Aiyktau, above Goranty and on the left occasionally vestigial stipules are early falling- Leaves 

bank of the River Vakhsh, between Kurgan-Tyube and rounded, or somewhat ovate, 3-8.5 X 2.3-8 cm, 

Lechman. Limestone, sunny rocky slopes, and sandy somewhat fleshy; leaf veins not prominent; base 

substrata;from600 to 1500 m. Also in iheKafimigan, rounded, sometimes cordate, apices obtuse, some- 

Pani, and Amudarya river valleys, in soutliwestern times obcordate, rarely acute; mucro lacking or ver> 

Tajikistan (Anonymous, 2005). 

small, 0.1-0.5 mm; petioles long, 1-2.5 cm. Flower 

According to Regel (in sched., LF), the fresh buds rounded, rarely acute; floral pedicels thick and 
flowers display a corolla with yellowish tints, and the long, 5-8 em; flowers slightly ^ygomorphic; abaxial 
staminal filaments are reddish. The dried fruits are (odd) sepal slightly galeate, 1- 

1 .5 cm long, 0.6 


Annals of the 

Missouri Botanical Garden 

().^5 cm deep; slameiis 'M) [o 80, aiilliets 2-1] mm, vvilli 

a ln-aiicli wltli a young (Viiil) of (Aipparis rupeslris iti 

rDiiiuI apires. Kriiil ellipsoidal \vi[li apices nipple- one sheel of the Sihllieipian Ilerhariuni al OXF 

sliaped, i)nlp red: ripe seeds dark lnown. ."5. 2-3. 6 X 
2.,S-:5 X 2.8-3 mm. 

Illuslralions. Kigutv 1 in All tK jnfri (19*,: S). 
Cnerau & Tones (1 98 1: 31). 

Phenology, Klo\verin<i; from May lo Octolier. 

Dislrihution und hahifof. Medlpa-ranean Region. 
Mcdllerranean iMuope and Noiili Alriea [Alba ma, 
Algeria. Crealia. Greece. Ilaly, Mhxa, Malla, Spain, 
Turke\]. iioeks, clilTs, walls of old huildings, at 
elevations frorTi lo 600 m, often sun 

oundnig human 

dwellings. Figinc 4-. 

Cdpparis oricnldlis was described hy Veillard in 
Duhamel (1801; 112), a|)|)arent1y fundauK^ntallv 
based on the pre-blmiaean Hlerature. lie giv(^s three 
synonyms, listing th(^ authors and ref<^rences \vhere 
these have appearetl ])re\iously. Also, fiulher malerial 
is cited in pages 142-143, after the discussion of the 
sp(H4es. The reha'cuccs lo the habitat anil distribution 
are reslricled lo: "Les rochers de Tislc do Crete et des 

corresponding to th(^ Fj. Grace. Pi'odi-. \'ol. I: 355. 
1809, number ] 190. which is also associated with 
H. fa-;iee. J. 487. The sheel of Cfipparis rupeslris is 
a v(aT l)plcal one from the Siblhor|)ian Hfabaiium. 
The cited illustration |Tah. 487] w^as later jiublished 
(Smidi, 1825); howev<M-, it is also oi-iginal ni;iterial. 
4 he eilation ''Folia (|uam In piaecedenle ciassiora et 
succo pleiiiora. ()li\!(^r'' is certainly ()li\icr (1801- 
1807). Guillaume Antoine 01i\'ier was a French 
natin-;dl>l who tra\(4ed in Greece, Turkc\ , ihc Ft^vanl, 
and otlier Middh^ Faslern eoujilries between 1792 and 
1798>. Therefore, lectotypification is ne(vl(Hl. We have 


eontaius neither rereienc(^s lo localities nor col- 
lectors, llowcxcr it is (dearl) laheUed "C. rnpestris/ 
Sib." [written in ihe hand of J. F. Snnlh] i\u<\ "J. 

None of the malerial has tlu? 

seen the slicet (OXF) witli the lectotvp( 



ccJie c 


isles de I'Archiptd, parliculierement 

|)an)s; en Syrie et dans la Palestine." Hodi localities 

and bibliogra[>hical references — in( hiding ilkkslra- 
tlons^fui'uish (undanuaital elements for (hHerminina 

Sibdiorp, M.D." 

]o<'alities written dire<-tly ofi the sIk^cIs 
Siblhorj)ian Herbarium al OXF.] Tlie spt:fimen is 
typical ol a specimen eolh^cted on ihe first \it\ag(^ 
in I 78>6 or 1787 (S(a-(aia Vlai-ner, pers. conmi.). It is 
in agicement with the descri|}lion in the prot(yloi^iie. 

41ir sh«'(M contains hntJior stamp and annolalion 

,1 ■ ■ 1 . ■ I /■ \7-\r"\'ri ," "V'""""n' ^^''^'^ reference to lli<' Frodromns ITora Graeca huKhMl 

the orignial material of Vedlard. Ihe author luniself i ^, * , -, ,- r. r ■ 

1 |-,Y- .1 , -1 , r^ r '*y '^'- ^- Fawson, ^^lierardian Frolessoi' ol liotanv al 

j)laces (lillcrent values on tlie malerud used. Part of 

the material is (tnly indir(M-|ly cited in tlu^ discussioti 

aftei- the protologue, in which stnnal additional 

authors, localities, and icon are cited. 41ie 


Ox lord (Pack, 1997]|. There ror(^, the specamen is 
reas(tnnbl} original material and is designat<'d liert^ as 
a leclot\po. 

spe(M'cs is not llhi^iiaU-d in the original pa|>er. 
Veillard's herbarium is unknown l)ecause it was 
apparently part of the missing Dniiamel herbarium 
(Sladeu & Cowan, 

1970). Ilurs the onlv ori^rinal 

nuiterials available lor lypificaliun are llio two images 
( iled by Veillard. Tl 

Scleclcd spcciftiefis rxftminc/L AI.I>\\1\. InMiik Saran- 

(hi. KrviidI s.fL (C); SaRiiidr'. \lshw 22 Hi (K). AlX.KKIA. 
Capr CaduMi, Bfjaia, Duris .12061 (F). CI{()\TI \. Cavlat. 
/.(irsen s.n. (C); Fapad, t)iihn)\Hik, fjirsen sjt. (C); Onhioviilk, 
Clrmrnl s.n. (UNC). (;|{FFCK. Argolis, PoKmi, II 


le remaining rcferenecs arf 

mnllnsti-att'd. FothctaV icon (FoniefM", l()79: 100) 
ma}' L)e discai'ded, as \'(allard hinisrU' nolod llio poor 
(juality of this drawing. However, it ehvirly re|)re- 
sents an unarmed caper bush ^\ith r()nnd(Ml leaves. 
41ie illustration in Bauhin el al. (1051: 03>) is cited 


by Veillard In the pre-Pinnaean 8ynon)niy of C. 
onenlalis and was s(4ccted as leetotvpc b\ Pi\era et al. 

According to \ (allard in Duhamel (1801). this 
s])e(4es was col Km -led in Palestine and Syria by 
tia\(4ers such as Pockockc and Shaw. W(^ ha\<^ not 
[(tund any [ihml material of this spetaes fi-om tl 
Pevanl. neither from these collectors 

f)S()7 (HN(;): Karpallios, Islet Solvastro, Darls H:iV>2 (K); 

Sukastro. I)i>decanf\s('. 77;. Rhus ,H:jH2 {\\K Kiklailrs 
Andros. Jury 271 (RXCl: Corfu. Maikos. Dfin's 51337 

(K); (ATolinuMias. 2H:i79 (C); Island ZakMilhos. J]i>nfi\nshi 

72H (CJ; P,.rl Klirli, Lens 612 (K); Rhodes, M,<iussrn s.n. 
(C). ITALY. i-'lon'Hi'r. s.n. (C); i^airrnio, l{. Coll :>'/■/ (F); 

I'iM-iigia. Ransone 410 (K); Pisa. .SV//7 429 (Kj; Momr-, 
Lnrseii IH74 (C); Sicily, Taormina. Island Im-ILi. Osfrnfrlil 
s.n. (C); M(\ssina, S. I\ Rroohc.s 5754 (KN(i); Fn\ignana. 
Ca]M- (^ilarossa, / R. Akern)(I 515 (1\\G); IsIaiiJ Ivian/o, 
Dnris 10171 (li\(.). I.lin \. Coefla, N of Bni^lia/1 Dnrls 

5()l77\Kj:i',e\uA \iAin\^^ii. Dnris 49670 [l]); Koiif,/ //. If. L 
26 (K): Sliahat. Mi 621 {]■]). \l \l,TA. Addaloiitc C-M.ulrrv. 


nor OLlitas. 


However, it is liktd) ihal the species oeenricd in tl 

Lunfnuuu 59bi (RXC); Malta. IFngA/ ,s.//. (kj. SPAIN. 
Aliranle: Cnini 2039 (C); Santa l^aHiara Casth-. hn>ccneio & 
AlrnrazOOOm (Mt4^). Haivoloiia: Barveluna. .SV/y//r/; 1 5H7 
(liNC;). IMza: Santa Fnkilia, Cannon 3256 (1{,N<J). Mal- 
lurca: l^ilnia de Mallnrca. Inncrnein t^- Alcnrnz 4H696 



Th(M-e is no desi«;*nation of liolot>j>e h)r Copparis 
rupeslris Sm. Serena iVIarner (pers. comm.) did find 


a snit^ie specnuen 

(one l:)los; 

soniin*i, branch and 

(ML b); Aicudia, Innrenno &■ Alcaraz RUyOJ (Ml H): 
\'atl(l('ni()sa. Jnrokscn s.n. (C). Meiiorra: lunula \ali. Riin 
s.n. [W'SC). Tiirragona: Ininfau-t, Jnoccnciif ^ Ahaniz 
4H70I (MFB). Valrncia: IJiria, Ininemin <Sc Aharaz lH70i) 
(MIJH). 'IlliKEV. Mii-Li Province, Marniarls Distiid, 
I'vinnv 1 16 (F). 

Volume 93, Number 1 

nocencio et al. 

Revision of Capparis Sect. Capparis 


6. Capparis ovata Desf., FL Ailant., Vol. I: 404. s.n (Ky |rIt3YA,Coena Benghazi D^^^ (RNG); 

^t^^ ,. . . T /T^ rxD .. (Jebel INefoussa, Gia(](). Davis 496/8 (RNG); Tripolitaiiia, 

1 /98. Capparis spinosa L. var. ovata (Desf .) Batt., ^^^^^^^^^^^^ j^^^^,^ jo38 (K). MOKOCGO. Driouch, Inocencio 

in Batl. & Trabut., FL Aigerie: 82. 1888. T\PE: ^^qq2() (MUB); Gorge du Ziz, Er-RiichKlia, Jury 17H19 
[Algeria] "'Habitat in fissuris rupium prope Oran'' 
s.c. (lectotype, designated bere, P 948!). 

(RNG); Fez, Matcos 6653/95 (liNG); bnzofirone, Jury 15602 
(HN(;); Msemrir, Dades, Jury 17776 (RNG); Nador, 
Kebdana, Rof7io 6501 (RNG); Ouarzazale, Brooks E.5349 
(RNG); Dj. Sarhoro, Ouarzazale. Davis 53476 (F): River 
KKvroTHESuiSPE(JKSOFCi/TO/?/5 0r.4r..MNTHKMRl)lTi:inn Yanoile, Inocencio 60021 (MUB); Safi, Inoceucw 60024 

liRcioN, THE MiDiii.i; East am) Ndtrni Africa ' 



Young leaves usually ovale to ovate-laneeolate, 
mature leaves ovate, 2.5-5 X 2-4.5 em; slipules 

(MUB); Taroudaiint, Jury 14453 (RNG); Taza, Jury 8602 
(\\NG); Sidi Belkassen. Ratherjord s.n. (RNG); Tiiaiit, 
Rutherford BV1281/93 (RNG); Tazeka, Jury 16777 (RNG); 


Younii leaves usuallv lanceolate, mature leaves 
ovate4anccolate. 2.5-4 X 0.9-1 .9 em; stipules 
retrorse b. C. omta subsj). myrlij'olia 

anii-orse a. C. ovata subsp. ovata Zaio. Inocencio 60000 {M\J\i). TUNISIA. Kabylia, J^'tournenx 

s.n. (P); Khargued, Letourneux s.n. (P); Fedj el Kbeirs, 

Lctourneux .s\n. (P). 

Tbe sbeet 948 at P contains two brantdies witli 
leaves and without flowers or fruits; the specimen to 
the right is selected as a lectoiype. It is labelled as 
^'Herbier de la Flore Atlantique/ done an Museum par 

Distribution. Figure 2. 

6a. Capparis ovala Desf. subsp. ovata 

^ ■ • 7 x^ n 7 ■ r> T ■ \ ■ h Desfontaines/ N"/ Cai^paiis ovata. '^ Another lal)el 

Capparis sicula \eill. var. kruegeriana Panip., L Agncoltuia LfCbiuMuunr. / v.a|^j a 

Col. 22: 459. 1926. Capparis spinosa L. var. rupestris states ''Habitat in fissuris rupium prope Oran." In the 
forma kruegeriana (Pamp.) Pamp., Prodr. FL Cireii.: prolologue, Desfontaines also cites seven pre-Finnae- 

an references associated vvitli images of a Capparis 
sp(H-ies known since at least th(^ 1st century AD from 
tbe coasts of Marmarica (nortliern Libya and Egypt), 

234. 1931. Capparis spinosa L. subsf). orientalis (Veill.) 
JaLi. var. knwgeriana (Pamp.) Jafri., Flora of Libya. 

Vol XIL L 1977. 

Shrul:) pendulous, sometimes reaching great dimeti- ^vhicb is without doubt Capparis ovata s. str. However, 
sions in shaded sites; twigs straiglit, up to 3 m long. ^^^|^^^. .;^Lithors interpreted these as belonging to C. 
dark green or with a reddish tint in young(n- twigs, spinosa or C. sicula. 

adult ones becoming woody, acquiring grayish or 
brown color; internodes 1.5-2.5 cm; stii>ules curved, 


Candofle (1824) raised the question of bomonymy 
itli Capparis ovata M. Bieb. On account of this 

mostly antrorse, somctiuics spreading, not decurrcnt, supposed homonym he proposed naming llie species 

sometimes veiy small or early falhng. yellow, 0.15- ^^.^^^^^ Algeria vvitli the type material by Desfontaines: 

0.4 cm long, up to 0.1 cm wid(; at the base. Leaves Qapparis fontanesii DC. Prodr. Vol. I : 245. 1824. 

usually ovate, when young ovate to ovate-lanceolate, 'pYPE: "in fissuris rupium Mauritaniae prope Or- 

2.5-5.5 X 2-4.5 cm, subcoriaceous; indument lax, an. . . v.s. sine 11. in In DesL" There is no reason to 

trichomes thick and short, 30-40 X 200-250 |lm; leaf ^j^^^^ ^|^;^ ^-^^^ ^^^ CandoUe because C. ovata M. Biel). 

veins not prominent; base usually rounded or -^ .^ ^^^^^^ homonym (Bieberstein, 1808). 

somewhat tapering, apices acute; mucro small, 0.5- 
1 mm, straight; petioles short, 0.5-1 cm. Flower buds 
acute; floral pedicels thick, long, 4.5-6.5 em; flowers 
slightly zygomorphie; abaxial (odd) sepal slightly 
galeale, 1.5-1.7 cm long, 0.7-0.9 cm deep; stamens 
30 to 80, anthers 2-3 mm, with round apices. Emit 
olmvate, pulp yellow; ripe seeds dark brown, 2-2.2 X 
2.2-2.4 X 1.6-1.8 mm. 

Illustrations, P. Ozeiida (1991: 246, fig. 08); 
Lewalle & Montfort. (1997: 25); A. Bencbelab et al. 
2000: 147); Charco (2001: 283). 
Phenology. Flowering from April to December. 

61). Capparis ovata DesL subsp. myrtifolia Ino- 
cencio, D. Kivera, Obon & Alcara/, subsp. nov. 
TY4^E: [Chad] 'Tdabitat in fissuris rupium Enneri 
Gousa, Tibesti, 3000\ 15 Mar. 1953, Cnichard 
KG/r/B/4(r (holotypc, the specimen with the 

label '1vG/TIB/40^ P!). 

Foliis angustis lanceolatis, stipulis valde retrorsis a typo 

di fieri. 

Shrul) pendulous, sometimes reaching great dimen- 
sions in shaded sites; twigs straight, dark green or w^ith 
a reddish tint in younger twigs, adult ones becoming 

Distribution and habitat. Saharo-Ai'abian and vvoody, acquiiTUg grayish or browm color; internodes 

Mediterranean Regions. North Africa [Algeria, 1 .5-2.5 cm; stipules curved, retrorse, not decurrcnt, 

Libya, Morocco, Tunisia]. On rocks or walls of old 0.2-0.4 cm long, up to 0.1 cm wide at the base, 

buildings, at elevations from to 2000 m, often in tbe Leaves usually ovate-lanceolate, the young leaves 

vicinity of human dwellings. 

Selected specimens examined. ALGERL4. Ahaggar, Tez- 

usually lanceolate, 2.5-4 X 0.9-1.9 cm, subcoria- 
ceous; indument lax, tri(diomes thick and short, 30-40 

zeit, 1750 m, Maire 180 (P); Bejaia, Rererchon s.n. (E); >< 200-250 ^tn.; leaf venis promment; base somewhat 
Djanet, Tamti of Tafalelet, Uwte 107 (P); Oranais, Faure tapering, apices acute; mucro small, 0.5-1 mm. 


Annals of the 

Missouri Botanical Garden 

straiglil; p(4i()les sliort, 0.5-1 rni. Flower l)ii(ls acule; 
floral pcdicelri ihick and long. 4.5-6..S cm; flowers 
slightly zygoniorphic: ahaxial (odd) se[)al slightly 
galeale, 1.2-1.5 cm long, 0.5-0.7 em deep; slameus 
30 lo 80, anllu^js 2-3 mm, vvilh round apices. Frull 
oho\'al(% [)nlp yellow: ripe seeds dark brown. 2-2.2 X 

2.2-2.4 X 1.6-1.8 mm. 


Fruit j-uujidcil: Iwigs yeiiow green Ut gnu -while; 
niaUire lea\es <)l)()\;ile lo o\ ale-iounded, 0.7-1 X 

n.r>-l eni; [iiihesetMice tlense 

4 ^ 

e. C. pdiiijlont suhsj). s/flidcrocarpn 

Distribution. V\ 

gnre 5. This d 

Ph('ii()h)gy. Fl 

owering Irom (SeptemI)er)Januarv to 


Disfrihntiofi and hdhilnt. Saharo-Arahian Region. 
Noiili Alrii-a [Algeria, (diad). On rock ere; ices, frotn 

1000 to 2000 m. 

The (lnj)j)(ins ovata po])n]alions of die C(Mitral 
Sahara mountains show disliiu'l n^trorse slipules (as 
most s])ecies in section Otpparis) in eoTilrasl lo C. 


(ipparis species 
shows a geographical pattern of xariation. 

7a. CappiirLs iKirxill^n-a Boiss. sultsp. par^illora 

Cappurls murniyann Gialiani, Cal. PI. Rnnihav: 0. M]l]9. 

T^ PK: [ItidiaJ ^^Oii veins of liaj) rock in the bottuiii of 

ravines al Mahahleshwur [Maliahalesliwar], rare; at 

Foghur (>'/r ('. Mavolm) - aheiil lliiri} chutiderjee [Dr. 
Gibson)"^ (not seen). 

Shrul) pnxannhent, np to 75 cm high; Iwigs straight, 




oratd {)opn1ations of Norlh Algeria and M 

have moslly atilrorse, sometimes s[)reading, not 


rrenl, sometimes vta-y small ov earl> -falling 
stipules. Tin; type of slipnles is a (diaracUer ver\ 

IIJ-) to 2 m long, light green or )edowisl 
intertiodes 0.5-1 .5 cm; stiptdcs somewhat eLir\'ed. 
relrorse, not decu rrent, golden yellow, contrast ing 
with the iuigs, 0.3-0.5 cm long. 0.1-0.2 cm wide al 
ihe hase. Leaves o\ate-rounded, 0.5-2 X 0.5-2 cm. 

distinct and constant. The leaves are narrow(M- and Ihe ''t'^-haccous; indnmcait variahle from dense to lax. 
lloral p(M heels are loiiger in the C(Mttral Sahara 



s thi 

s])ecitnens. This led ns to distinguish this new 

n and long, 20-25 X 3()()-00() ).im; 
u\i( \eins not ])r{)minent; hase acute to taptning. 

subspecies, that is subordinated to C. orata. Other- ^^1'"''^'' rounded or acnie; mucrn very small, 0.1- 
wase it has some likeness to C. carfihigiiwa Deem:'., ^^"^ '^^'^^' straight; petioles very short. 0.3-0.5 ctn. 


wdiieh is also |)resent in the area, but the strongly 
zygomoiphic flowers of the latlei' species (whi(di we 
in(dnded in another section) are not found in C. ovata 
subsp. niyrtlfoUa, 

Ptiraiyprs, AI.(;i^KtA. Dartnouilly, W of Tanianrassel, 
Chipp 2R (K): Tarnaiirassel, Chipp 28 (P). CIIAI). Aou/I. 
Tihesti. Dalloni s.n. (P); FniKM-di. Tihesti, Dullnni s.u. (P); 
Cozoii, Fiiiierili, St. Se/olc 57 fj-): Gorires I/Ondin^nieur 

■■ ■ o O ^ 

Tdn-^ii, Brook! 32 (K): Fnneri Gousa. Tthesll. lOOO ni. 

(luictuird sji. (P). 




)uus r(tnn(ic( 





suirniiy acute; ll(Ma 

pedicels slender, short, 1 .5-2.5 cm; (lowers slightlv 
z)gonioi-p]iie: abaxial (odd) sei)al slighll_\ galeate, 1.2- 
l.I cm long, 0.5-0.6 cm (lc(^[); slanu-ns 30 to 80, 
anlh(Ms L3-1.5 mm, with round apices. Fruit oblonu, 
pulp red; ripe setuls brown, 2-2.2 X F8-2 X J.6- 
1 .0 iiini. 

7. Capparis par\in<n*a Roiss., Diagn. PI. Orient., 
Ser. 1, \o]. I: 4. 1 813. Cappans spinosa var. 
parrijlora (Boiss.) Uoiss.. Fl. Orient. Vol. 1: 420. 
1807. Capparis UmcophyUa DC. var. paniflora 
(Hoiss.) /ohary, IJull. lies. Council Isiael 8 D: 
59. 1960. TYPE: Ihan] "llab. in P(asia anstrali. 
Aucher pi. rxs. V" 1I<)I cl 4191 4" (h^etotype. 
designated lun-e, G!, (;r>503). 

Phenology, FIoutM'ingand fruiting from (April)Mav 
lo Se])tember. 

Distribution and liabiiaL Irano-Tnranian 
Saliaro-Arahian Hegions, extending to the Stidano- 
Zambezian Kegiim. Middle East and Central A>ia 




Pakistan, Saudi Ai'abia, 
l'urkm(M-iistan]. Cliffs, stony places, and slopes, in 
semi-deserts; ftom 6.50 lo 1850 m. 

A holotype was not designaUnl for Capparis 
mnrrayana Graham (1839). Tlie John Graham Her- 
barium has not bemi found. 

l\v\ Toutt: Srusri'CiKsor C\i'i'i(a:^ r\R\n-'ijnr\ ix riir MinnrK 
East wo (a:\nc\i. Asia 




Fruit oblong or tdliplieal; twigs ytdlow grc(M); 
niatLiic leaves u\ ate-roiitid<'d. 0.-5-2.5 X 0.3- 
2 eni, ptihescenee from deiihc to ahiiosi glal)rous . . 2 
iMMiil oblong; nialure li\ives ovale-rouiidi'il, 0.5-2 
X 0.5-2 eni; piihes<'enee fvnm dens(^ lo lax 

a. C parvijlont snhsp. juirrijlont 

Pruil ellipsoidal; mature leaves ovale-laneenlale, 

randy ol)o\ate. 1-2..") X 0.7-2 em; pul)eseenee 

ahnost glabrous b. C pmi'ijloni subsp. hunlica 

Si'brtcd .specitiicns cxutnined. AbC!! ANtSPAN. I leral. 
Ihilgc S: Lamoud s.n. (K); Kaiukiliar Tu'/ada, luidbcr^ 2()32a 
(F): Kaiukihar Pir/ada, Hedge <K: lj!nn>nd 2052n (F); 
Kajalvay, Petcrsm 452 (F): Kajakav. //rr/^^-e &■ fjinmnd 

2hl2 (C); Proxinee of ( :iiakliansiir, 2 km In llie N of Fashe 

Jona)n, Breckle 1921] (F): Shin Dand. 10 nn. S. Fiuse s.n. 
(K); /inl Gorge, Mam dislriet, 8 June 1038, CInipnum 26006 
[K). lliAN. Kars, Knli-i^8amus, "^rh'mxs^ An hilndd 2910 (E); 
Knli-e-IIari. A, ./. Ire lli (K); Sehiias, Kofseliy .V)9 (K); 
Selnras, Ilofwnarlrr 509 (C). PAKISTAN. Tafido Jan. Jo/ri 

2106 (F). SAUni AKAIJIA. Aflja Well, ,/. /;. Dmvr 15125 
(K.NC); Turayf, Cnllrnrlir t195 (K). Tl P.KMFMSTW. 
Ashjabal. s.n. (la. 

Volume 93, Number 1 

nocencio et al. 

Revision of Capparis Sect. Capparis 


71). Capparis parvillora Bolss. subsp. kunlica bases lapr'riiig to rounded, apices rounded or weakly 



bioceneio, D. Rivera, Olion & Alearaz, aeuLe; iiiucru 

very small, 0.1-0.5 mm, slrai<ilit; 

slat, et eoiul). iio\ . Basioiiym: Capparis ovata petioles veiy short. 0.1-0.3 em. Flower buds rounded; 
Desf. var. hiirdira Zoliaiy, Bull. Res. Council floral i)cdicels slender, short, 1,5-2 em; Howers 

Israel, Vol. 8D, 56. 1900. TYPE: [Iraq] "Rupes sbghlly /Agomorphic; abaxial (odd) sepal slighlly 

galeate, 0.8-1.1 em long. 0.3-0.6 cm deep; stamens 
30 to 80, andiers 1,2-1.5 mm, with round apices. 
Fruit rounded, pidp red; ri[)e sec;ds dark brown, 2.6- 

Mt. Singarae [Djahal Sindjar], Mai lc>67 C. 
Uausskncchl s.n.^' (hololype, K!). 

ShrL[|j procumbent, almost glal)rous; twigs straight, 
ui) U) 2 m long, yellowish green; internodes 1.5-3 em; 
stipuh^s somewhat cur\'ed. retrorse, somewhat to \ (My 
widely spreading, no! deeurrent, go 

2.8 X 1.6-1.8 X 2.3-2.8 mm. 



PJieaola^'v. Flowering and fruiting from (Apiilj 
May lo .\ugu>t(September). 

Distrihiiiiofi and habitat. Irano-Turanian Region. 
0.1-0.2 em wide at llu^ base. Leaves ovate-lanceolate. Central Asia [Afghanistan, Turkmenistan]. Clids and 
rarely o])ovate, 1-2.5 X 0.7-2 cm, herhaeeous; ^|,j,|y slopes, from 600 to 2000 m. 

contrast ing with 

the light twigs, 0.2-0.4 i-m 


leaf veins not prominenl; base rounded <tr somewhat 

The sheet with the hololype (al E) is labelled as 

Paralypcs. AFGHANISTAN. Chakliansur. /nraiij, 
BrrrL-h' PJ2H (E); Fariah. Hedgv, Wcndelho & Ekbcri:: W 
7674 (K): llenit. Hedge & Lamoiid :U579 (K); Shind Dand. 
Furse S411H (K). TERlvMEMSTAN. Asjahad. "Sddiin & 
hiinoi s.n. (F). 

ta|)ering, apices acute to rounded; mucro very follows: I ^^K.ll. Reehinger, Iter Orientale 1967/ 
small. 0.1-0.5 miTi, straiglil: petioles very short. 0..3- 37579/ Capparis spinosa L./Var. parriflora (Boi>s.) 
0.5 cm. Flower buds rounded; floral pedicels Rniss./Sw-Afghanistan, Herat:/ 1 05 Km S Herat Ver- 
slender, short, 2-3.5 cm; flowers slightly zygomor- ^^^^ Shindand, 1300 M." 11 ^T)et. Hedge & Eamond, 
phic; ahaxial (odd) se[)al slightl) galeate, 0.9-1.2 cm 1950/ yyiTl." 
long, 0.1-0.6 cm dee]); stamens 30 to 80, anthers 1 .5- 
1.8 mm, with rounded aj)ices. Fruit ellipsoidah pul[) 
red; ri])e seeds dark brow n, 3.2-3.8 X 2.2-2.6 X 2. 1- 
2.2 mtn. 

Plicaology. Flowering from June to Seplember. 

Dislrihuiion and habiial. Irano Turanian Region. 
Middle Fast [Afghanistan, Iran, Iraq]. CMffs. ravines, 
in slony places, from 200 to 700 m. 

Seh'cled speeimeiis exiuidaied, AlGHANISi A\. Clia- 
khaiisur. Zaranj. HrecUe l<)f)5 (F). iKAX. Avrumaii. Sclialui. 
Ilaiisshneihl s.n. (K). IRAQ, liilas, Raui 291(19 (K): 
Dar\icli[vliaii, I5:'>6 (F): ZinI ^^ov'^e. Mam dish-icl, Cliapntan 

Tc, Capparis parviHcna Roiss. subsp. si>liaer()- 

rarpa Inoeencio, D. Rivera. Obon & Alcaraz, 
subsp. nov. T^ FF: [Afghanistan] ^•|leral:105 
Km S Herat versus Shindand, K. II. Rrrhmger, 
Iter Orientale 1967/37579' (holotypc. E!). 
Figure 6. 

loliis MiiiK)rihu.s, usque ad 1 ctti longis lalis{[iic. Iriielihus 
hicviorihus <!;lol)osis 11011 oljjongis a typo diflerl. 

8. Ca|)paris sieiila Veill., In Huhamel, Traite Arb. 
Arbust., Ed. 2, 1: 159. 1801. Capparis mala var. 
siciila (Veill.) Zohary, l^idl. Res. Council of 
Fsratd. 80: 55. 1960. Capparis spinosa sul.)sp. 
sicula (Vedl.) Holmboe. Borg. Mus. Skr. Ny 
Raekke. Bird 1, 2: 1-344. 191 1. TYPE: [Italy] 
"Capjiaris Sicula dupllcata sjjina, folio aculo. 
Boccone, 1666 [1674]. Icon, et descripl. Rarior. 
I^lantar. Sicll. P. 79. tah. 42. f. 3. Cupani llorl. 
Cadiol. P. 36'* (leetotype. designated b\ Rivera 
et ah. 2006, Boeeone's image, Icones et 
descriptlones rariorum plantarum Sieiliae, Mtdi- 

tae, Juliae et Italieae: 79. lab. 42. F 3. 1674!). 

Shrul) [)roeund>ent, up l(t 75 c-m high; twigs straight, 
up to 2 m long, yellowish green or grayish-whilish: 
voun^ twi^s verv thin with very short inler[iod(\s (0.1- 
0-3 cm) and very spin\: longer adult twig internodes 
0.3-1 cm: stipules som(^whal curved, relrorse, usually 
very open, slightly spnvuling to widely sprt^ading, 
slightly deeurrent lo not decun-ent. golden yellow 
contrasting with whitish twigs. 0.3-0.5 cm long, 0.1- 
0.2 cm wide at the base. Feaves obo\ate to o\at(^- 



F the vouuii roundec 

led. 0.7-1 X 0.6-1 em, 

herbaceous; indnmeni dense, trichomes thin and long, 
20-25 X 350-800 |.lm; leaf veins m)t prominent; 

K\\ ro riiK Si lisrKciKsor CArrAiassici l\ imiii: \lKniri:i{U\M:AN 
Rf.(,io\, Noirni Aikicv, tue Midnm; F\sr. vm) Cfatkai, Asi\ 

la. Plants with stipules straight, spreading 

8h. C. sieidd suhsp. Jjerfuiren 

11.. PFuils with stipules curvrrL retrorse 2 

2a. Feaf puheseenc-e lax. very la\. or almost glahrous . 3 

3a. Twigs dark grei^n: leaf juihcscciicc lax. trichomes 

thick and long, 20-50 X 100-800 jim; Roral 

|n'ilir(4 lliiek and long, 7^.^-7 em 

. Hi\. C. sicula sLihsp. sieida 

31). Twigs light green, while, or \ellow: leaves 
glahrous or with \ery lax puhesi-cuc-e, trieliomes 
ihin and sliort, 15-20 X 100-250 l-Ua: floral 
pedicel slender and short, t— F5 cm 4 

4a. l.eaf puheseence veiy lax; stijjnles curved, rc- 
n-ors(!, y(;ll()\v-orange; antliers siiialL 2-2.5 mm. 
8d. (i sieidd SLihs]). mesopoiamiea 


Annals of the 

Missouri Botanical Garden 




Lt'af ii]tih)sl <^lal)i(Uis: sli[ui1('s sninrwlial cinvfil, 

reti'orsc oi- spirading, gt)Id(Mi yf'll<'\\ ri)ji[mstitig 
willi [he liglil color (){ Iwigs; aiilliiM-s \ cry small, 

1.6-2 iniii 8f\ (I, sicitid siihsj). sinrlidna 

Lea\'es a[)|)carinu while dut' In ih'iisc piihcsceiife 

Dislrihitlion. I 

'igiirc 5 

Valiiniii, IVlopotiossos. Ihinson 67-1-1 (HNCj. ITALY. 
Hiisilicala. Po\cnzi\, Akcroyd 3.12i^^ iHNC): (iigciii. Agrigciilo. 
Taraliones.n. (C). MOlU K :( X). Imv. Jmnrnno 60( 1 1 f) {WV \l): 
KlirnlrhM, Inoccncio 60011 (MLIJ); Mi-kia-^, Jury J 5302 
{\l\(:y. Sidi-Karccn. fmxrncio 60017 (Ml'B). SPAIN. 
Be. C siciild siil)s[i. U'lu-djilnlld Alicaiilc: Heser\oir of Ainadoiio. Mcdiiiz 1H705 (Ml W): 

La Algucfia. Crcvillriitc. Inoccncio <K: Mcarnz IHOH'i (MUR). 

Al.iH'i-ra: Santa Mana dc .\icva. David I0J7 (KNC): Ni'iar, 


}{a. Ca[)paiis sicula yubsj). siciila 

Ciippdris spinosii \ar. cdnesccns (^oss,. Anal. Sci. ,\al.- 1 I: 28. 
1849. Capparis spinosa >iil)sp. ctmcsccns (Coss.) A. t(' 
0. liolos. Misc. F(Hits(M-e: 8<>. I^Ol. (Aij)parls ovaUi 
DesL var. i-dncsccns (Coss.) |-|c\'\\ood. I'cddcs Hrjicfl, 

iK-cnrio lK: Akaniz 18/ 12 (M UB): IJcija, Inotcndo & 
Alc(tr<iz IH7J0 (iVU lij; (Canada dc Vric/, Orcf, Inoccncio & 
Alcaraz IH7II[\\V]\): Las (:nadia> dr I). Pepc, \ cic/ Kuhio, 
Inoccncio &• Alcoroz UU)H2 (Ml H); Los Lohos. Inoccncio iK: 
Ah-aroz IH72H (.MLB); Clnircli ofSalifMite. riiii-i\(d. Inoccncio 
iSc Alciiniz IH7I3 (Ml Hj; liucEval-()\ era. Inoccncio ^K: Mt^orttz 
1H72H (MLB)- Sen'm, lnoccncii> di Alcaniz ■i:i07ll [Ml W): 

69: 36. 1961. 'YWK: lS|minl "In nif>eslrilnis o[>piduli Sierra de (ia.lor. \ahlcs Hl.i (H\C). Cadiz: Jcnv. Inoccncio 
Buena\i^la [.lopc Xere/ {E. Boni-:cau. pL Esp. IHI9. cK: Alcomz s.n. (MUB): Sanliicar. N. Silrcsfrc 252I/6H (\\\C,). 

n. 4:if (lcctoI\[)c, designalinl licrc, PI). 
dopparis orolc var. palocslino /ohar), BiilL iles. Council 

Israel 8L): S^. PJ(>(). TYPK: | Israel] Lp]U'r Calilee, 
"\\"adi llindaj. 23 jinie ]9.")L,1/. Zoh(ir\ / //^ (hololvpc 


Craiiada: Caslillrjar, /'. /■'. Cannon 692 (KP^K;); iviaia. 
CardiHT 1337 (Ji.N(i): LanJaroM. linncncio & Alcaniz IH71H 
(Ml Bj; Bes(a-\oir of .Negi-alfn, Inoccncio ^ Atcaraz IH7(}3 
(Ml P>): (;nadix. Inoccncio & Alcaraz 4H712 (MLB): Loja, 
Inoccncio <K: llcaroz IllOHj (Ml B): Baxa. Inoccn<-io <S: Mramz 


■IHor.O (MLB): SaloLrena. Imncncio ,K: Alcamz AST/ 7 (MLB). 
lliiosea: Velilla de Cinca. lnocencii» S: \lcaroz IB6B8 
(Ml P>). Malaga: Torre del Mar, Inoccncio iK.- Mcantz IH6HH 
(MLB): V(de/ Malaga, hnwcncio & Alcaraz 48719 (MLB). 
lMallor<'a: from Palnia de Mallorea lo Andrailv. h}occncio ^K: 
Ahiiraz IH726 (MLB). Ihii-eia: SaiUa (an/ dc! CaKario. 
Lani^c s.n. (C); Alui-cla. l.anL^c sji. (Cj: \ cnta del ()li\o, 
Inoccncio & Alcaraz 13703 (MLB): Barinas. linncncio & 
Alcaraz 1 37 i ) I [\\l W): \\\)Ui\c\U\ I noccncui ^K: Alcaraz 13709 
(MLB): Lorea. Inoccnno X: Mcaraz 43722 (MLB): ^'^e|]a^ 
Imncncio & Alcaraz 1371 1 (ML'B). Jarii: Alcandele, 
Inoccncio & Alcaraz 48721 (MLB); from Lnrva lo Cnadiana 
rur\etl; [)elj()l('s slinrL 1-1.5 cin. l^d(t\\('r Buds aciile; ^'^<'^^^^^\ li'<*<'('nci() & Al((ir(iz 13727 (MIB): Jodiiv, Inoccncio & 

floral prdlctds lliick and 

Slirul) |n-()C!iinBcfil; lulgs straigliL soinctidios reatdi- 
ing up to I] m lotig, dark gixMMi; iiitrrnodos 1.5-5 cm; 
slipiilf-s ctii\(M], ixdrorse, not dcciinctiL occasioiuillv 
sllghlly deciirroiiL vidlou-orango, ()..'M).6 cm loim\ 

0.2-0.3 cm wide al llic base. Lcaxcs o\alc. oblong or 
elliptic, 3-5 X 2-1.5 cfu. hcrbaccoos; indumenl lax. 
tricliomes thick and long, 20-50 X lOO-JiOO j^ttn: ]rd' 
\eins not |)romln('til: base ronnilcd or somewliat 
la[)cring, api<-(^s acute; iiuicro long, 1-1.5 mm, iiSLially 

long. 5.5 

* cm 

: n 


zvgoniorphic: abaxial (odd) sepal galeale, 1.7-2.5 ctti 
long. 0.7-1.2 cm deep; stamens 100 h) 150, anthers 
2.5-3 mm. wilh acute apices. ImluI oblong, pnlj) led; 
ri[)e .seeds dark brown. 2.6-3 X 2. I-2.P) X 2-2.2 mm. 

llhiMnilions. Boccone (1671: 70, tab. 42. f. 3); 
/ohary (1966: 350); \aldeb el al. (1987: 374): 
Caslroviejo (4 ah (1003: 520, pi. 142); Pldmanti et 

al. (1983: 81); 0. Kragmaii cl ah (2001: 312-3. 
pb 133). 

Phenology. riowering May to ()id(jbci-. 
Disinhulioti (ind hahitdt, MedihM-raiiean 

Aharaz I8i20 (Ml B). Sevilla: Osniia. Inoccncio S: Alairaz 
18679 (ML B): S of Spain. ./. IL. Carr 20706.6 (HNC). 

S'^KIA. [)j(l)el Casioun. Damascus. .Sr/;n//?//('/,\A*y// /3//i(K). 

TrUKKV. Ankara. Dints X- Eoodc 37217 (1\): DardaiK-lles. 
>.//. (L); Ocni/li, a: Ilornda 333 (R\C): Kr/urum. Ollu. 
iloMop 14366 (L); llakkarl, /ah ri;er, Trelawny 1303 (L); 
Ke^jiliirkrnerih, M<-rsiti. Ilcnnipinan 107.'' (I^N(;); Painnk- 
kal(\ Dciii/li. Rayiop 10231 (Is); Saravcik-( )Mnaii( tk, 7n/;ey 

2309 (17j. 

Hl>. CapparLs sinila siibsp. herharra (W illd.) 

Inocencdo, I), Ri\('i-a. (Jbon & Alcaraz. staL et 
cond). iio\. l?asion\m; Cnpjxiris hcrlxn-ea W illd.. 

Kiium. Pb: 5()0. b*^.()0. C 



Irano-Turainaii I legions; locall) iuiiodue^Hl in the 

Saliaro-Arabian Ivegion. Mediterranean lMu-o|)e, North 

(ipjuins ovida \ai\ 


1. Middle Ivisl into Turke\ [Albania, Algeria. 
Cyprus, Greece, llalv. Morocco. Spain. S\ lia. Turke\]. 
Slony places, marls or cbu ish soils, scrubs, al 
elevations b-om to 600 m; in the \ icdiuty of human 

SelccU-d specimens examined. AI.BWdA. Pxlow l,c\ani 
and I'la^eida dislrid. M. Vrdv-dX. Baltiiui 197 {\\). ALCIIBIA. 
Oran, Eaure s.n. (K). CY141L^S. Cape Creco. Cold 29 (ITXCj. 
(d>F4^]CK. l^aths of Kretrta, l>lanil Luhoea. SiamfAtiatdtou 
/7290 (Cj: Crete. Kissamos. Biekcrich 130^)1 (Kj: Irakliou, 
Bourn 8913 (B\C); I'okis. Delfi. Pif,scl 107 {\lM7y Island 
l^)ros, Sn-id 29680 (C); Mililini. L.^shos. Hansen 4918 (C): 

hrrbacea (Will.!.) /ohary. Bub. bes. C 
Israel 8D: 56. 1060. TYPE: [Russia, (;(H)rgia or 
A/erl>aijan] "Cap>[Kiris herljacea. Marschall a Bie- 
berslein. Llahilal ad Caucasimi" (l(n-|ol\ |)e. 

ih^signated here, Bl, unlal 





sjictdrnen, B-W. fuldi-r 10034, right of slieel 2). 

Capparis hcrhacea Willd. \ar. ndcroplijlla Lcdi-h., \A. 
23.). 1842. (A/pparis leucoj)h\lla \){\. \ar. niicroplnila 

(behetl.) Taekh. Stndenls" Flora of Egvpt. Kd. 2: 164. 
197 L TYPE: |ka/akJi>Ian or Tinkmcnl-lanl "llah. ad 
hll. Orient. m. ('a>pii! Karelin" (holotype. l.E not seen). 

Slirtd) ])rocumbent; tu igs straight, som(4i]]ies r(^ach- 



lo 3 









uiteruodes 1-3 cm; slljiides slraighl, sprc^iding, not 

Volume 93, Number 1 

Inocencio et al. 

Revision of Capparis Sect. Capparis 





10 cm 



7i ^ cVv 


2 cm 

3j ev'fi/ 

2 cm 


6. Delciils of ihe ninv suhspccirs Capparis [Htrvijhyra siil>sp. sphnemrarpa liioctMicio, I). Hivrra, Olx'm, tK yMcaraz. 
— A, Stems aiuinowers (drawn by J. -A. HaiTcna Irotii Fursc 548H. K). —1^. Dclail of leaf ami slipulcs (drawn liy J. -A. liarrena 
from Nikilui & Ivauov s.n.., E). — C. Kniil (drawn liy J. -A. Barrcna [V(nn Hedge & Ltuno/id '>7579, E). 

Dislnbiitiun (ind IkiIjIihL Irano-Turaniaii Region 
extenditig lo llie Eiiro-Siherlan. Middle East, Ceiilial 

decuneiit, golden yellow, 0.3-0.6 em long, 0.1- 
0.2 em wide al the base. Eeaves elliptie or <»Itlong, 

3-6 X 1.-5-4 em, lierbaeeous; indunuMit lax, tri- Asia, and Caueasus [Afglianislan, A/erhaijan, 

eliomes thin and short to long, E5-2() X 2{)0-r)00 |.tni; (k-orgia, [ran. Kazakhstan, Mongolia, Tnrkey, 

leaf veins prominent; bases rounded, apiees obtuse to Tntknieriistan, Ukraine, Uzbekistan]. Stony plaees in 

aeule; niuero small, 0.5-1 mm, curved; petioles short, ealeareous soils and roeky grounds, slopes of low hills 

1-1.5 em. Flower Iinds acute or rounded; floral and walls of abandoned buildings, al elexations from 

pedicels thick anrl h)ng, 4—6 em; (lowers zygomorphie; lo 2000 ni. 

abaxial (odd) sepal helmet-shaped. 1. [5-2.4 em long, 
0.6-1.2 cm deep; stamens 100 to 1-50, anthers 2.3- 
3 mm. With acute apices. Fruit o]"}Ovate to oblong, pulp 
red: ripe seeds dark brown. 3—3.6 X 2.1—2.8 X 2— 





[)opidations display stouter 

stipules and smaller lea\"es. 

Illustrations. 4'akhtajan. (1966: 58, tab. 22). 
Phcnoloi^y, Flowering (rom Mav to Sei)lember. 

Seleeled speciinens examined, AF(d FVNISI^AN. Bamian, 
Oarrah Siakar. Hedge :il2:i (E): Dm Kiindii-. Edelhcrg 1889 
(C): Kundiit. Khatiahad. Carter 390 (K): Obeli, Ih^-at. Hedge 
W7777 (E); Samangan, Ileiier 1128 (E); Takhar. Mugliul. 
Podleeh n:i77 (E): Vawar/an. Badkslian, Hedge \\947I (E), 
A/EKiF\IJA\. Morghak, honi Far.sabad to Bil.-li Savar. 
Latuond 'ii)97 {\\]. {,\X)\\{A\. S.I.. Frierh s.n. (E): Caucasus. 
IlfdieiKudcer s.n. (iC); Tbilisi, Camphell 17.^ (K). 18 AN. Aniol, 
Andersen 211 (1^); Kli\(f\, Coutm J 560 (K): Mazandaran,, Fiirse ,K: Synge 491 (K); Mian.^h, Hoirles 2123 (K): 
Morawcli Taj)])*'!!. Heieer H3H01 {K): Sanganch. Kopcl Dagli. 


Annals of the 

Missouri Botanical Garden 

Choraslii-M-flnsseni lOr^C {\U]H}. KAZAKHSTAN. Tcliavlo- 
uru/i I()>hiir(' sr\. Tanicr l;iti()\ ski. Prinjln s.n, (K), MON- 



nun prdciimhriil: twigs siraight. sciiii-erect, 

COLIA. Tiati-Sliati, [\'lon^(tlia, l\>Uifiui s.n. (K); Easlcrn 
M{>ii<^(ilia, i',i)\)\, PfTZiralslii s.n. (K). TUKKKY. Arlviii, 

sonu'times re 


ng up 

to 3 


long, glaucous; 

tilcriiodcs lJi-.>(-ni; stipules cui'ved, rchxtise, not 

Conih. M//7.S <^ Ifnli^r MVl^/lV ( K); llakkari. Kalnlans. Dan's '!<'('t"''-^^iil Of soHK^what (Iccunvnl, golden y(dlow, 0.3- 

23fu0 (E): Kagi/iiiaiK \\<ilMm 'i75 (K): Karahiik. Bdxlop 
11383/65902 (E); Kars, Paris -16680 (E) (K): Koumi. 

0/) em long. 0. 1-0.3 eni ui(I(? al ihe hase. Eea\es 
elli[>lie \o roundefl. sometimes ovate, 2,S-1.S X 2— 

Ak^i.^kll^, Dural 3(6 (E); ()sinaiii\t'. Balls I IW (K): Sitiop. o ^ i i • i , i i •.• i 

-. ' . ' , ,,,,^,, \/ ,„ , ;,., ,^ . : / . : .' ."i.o enu nert)at'e()us; uidumeiit ven dense, whitish 

Knrgi. Tnhry 2809 (E); Tokal-Niksar. Dan's 21882 (K); 
Zongiildak. Kaiahiik. Dans & Coodc D390;10 [i:). TUIJK- 



s llti 

n and long, 20-23 X 200-300 j^lin; leaf 

MENISTAN. Asehahad, Frcyn 260b (E): Svr-Oaria, ColiLr \*'i'>'^ ^i"^ (nonilnenl; bases |-ounded. apices ol)luse tjr 

s.n. (K). EKUAIXE. Kr\in. Valla, Toi^rc Dl()6 (HNC). aenle; nuiero long. 1-1.3 mm. siraiglit or soniewliat 
L/iiEKkSTAN. Ah.M. Tcp.-. TashkeiU, 490 ni. \asak s.n. 

(K): {.'hamast, Sainai-kaiid, Daulscn 2/i (C). 

Then^ Is a clear reference in Hie ])i-oloh>gue to die 
Caucasus, which ininrecMy points lo die spfH-iniens 
(rom ihis an\i in [he herbarium T\^illdcnow (siupris- 

ingl) the prolologue does not menlion die Mussin- y. 2 6-2*^ X I 8-2 
Pushkin expedition, vi(L inlra.). The reference in the 

curved; petioles >lu)rl. 0.5-1 cm. El()\\er huds round- 
etl or acute; floral pedicels thick and short. 2.3- 
3.3 cm: (lowers /ygomoiphic; ahaxial (odd) sepal 
galeate, 1.5-2.2 cm long, 0.7-1.1 cm deep; slamens 
1 00 to 130. aiith(M*s 3.5^- Mini, wdh acide apices. 
Emit o|}lt)ng. [►ulp wd:, lipc >ced> dark brown. 2.7—3 

protologu*; lo a ^'('apparis herbacea. Marschall 
a Hieberstein" is presniiiablv poinling lo Cdpjxiris 
ovahi M. Rieb (bieberstein, 1808. 1819). In the 

llluslradons, MandavilK^ (1990: pi. 69-70). 

Pheuolo^y. Mowering fi'om Ma\ lo S(M)t(Miiber. 
Dislrihulnu} (uid liahilal. Irano-Turaniaii and 
lierbarium W'illdcnow (B) ar(M\vo sheets w ithin folder Saliaro-Arabian F\egions. Norlh Africa, Middle l^ast 
nr. 10031 pertaining to CdpjHiris herlxtccd (Hiepks, into Fakislau | Afghanistan, Iran, Ira(|. Israel, 

Pakistan, Saii(h y\rabia, Yemen]: also In l^gypt 

1972). Ihe h)l(ler is labeded: "PolyaiKhla Monogvnia/ 



Ca])])aris herbacea foliiis/ subrotuude elli[)licis ovalis/ (Zoliarv, PXjO). Oasis In semi-deserts. 

a\illis spin(tsis. PeduueuHs/ iiniriorl^/ Mabilal (^aiica- plains, sometimes in somewhat salitic soils: at 

sus." Sheets ] and 2 are nimibered and aufiolated both (^(nations from to lOOO iii. 

as lollows; "C. herbacea'' and ''W." The f(>ldcr has two 

(ttlier hibels: "Mussin Pushkin/ W.'* This refers to 

riie sheet wdli the leclolype t>( C(}j)j)(iris Iciicophylla 
is labelh'd: I "(!ap|)aris hHicoj)h\'lhi 0(7 {Di' Caudole 


CounI \[K)llo Apollos()\Ich Mussin-Pushkiii (1760- Scalpt.)" 11 '\le Hagad a Alcp./ Oliviei" de Ihugniere 

1805), who was a Russian ex[»lorer and plant III 'ilerb. VIiis. Pari^./ Capfiaris leucoplnlla DC:." Tlie 

collector. Ih^ led a iKtlanical e\[>e(lition lo die coincidence between lalxTs and references lo t\pe 

Caucasus in 1800-1802. The other label is almost malerial in ihe prolologu*^ led us lo suppose (^andolle 

illegible. It is not clear whether tlie s[K"cinien was was impllcllly designating a holol\pe, [)ro\ Idcd the 

originally colh-ctcd in the Caucasus by Mussin- author u^(mI oiilv one elemenl. 


Pushkin or, presumably, cnltixatcd in ihe Roval 
Polanic Carden of Berlin (mm seeds a:alher(Hl In thi.- 


collecloi" (die species Is [uiblished in a catalog o( 

planis actually grown al Pcrlin). This species w^as, in [Judak, [= \MAKurl\J)avis c^^ BnUi<in D. .V)30.1 (K). \\\ XQ. 

Srfccterl spccimrns cxdminnl. WVA IAMSTAi\. liaglilati, 
S\\ of ncshi. ficncr 1153 (K); Morghak. Fursc 7735 (K). 
IIIAN. Bam, Lco/iarfl 6052 (K); Krfuian. Parris 75!{)5 (K): 

(act, culli\ated In anothci botanic gaixk 

n in 


Petersburg: "Cultam in tepidario saepe frulicosam 

fieri et C spinosac asslmilari nuncial Else her in 

' I Vied rich fanst Pud w iii von Eischer was 




director o( ihe Im[>erial Botanic (iardcii of Saint 
Petersburg (Pritzel. 1872)| (Bieberstein. 1819). 

8c. Capparis siciila \'cill. subsp. leucopliylla (DC.) 
TruK'encIo, D. Rivera. Obon & Alcaraz, stal. (;l 
comb. nov. Baslonym: Cappari-s lcuc()j)hylla DC, 
Prodr. Vol.1: 216. 1824. TYPE: |ira(i] ^Tnl.T. 
Bagdad et Alep. Olif. rl Briig. (\'.s. in Ilerb. Mus 
Par.)'' (Icctotspc, designated here, P!). 

Ilanialu Knriii iS: \iian 39981 (\\): Tell Koh lirk-St'iional, 

Mosiil-Liwa. J. B. Cilln KfHlO [\\): Snullu-rn DrMil. S. of Al 
Salman. Rmi. Ai^nciv i^ Ffaincs 1656 (E): Shaikhiva. Saliiia- 
Samaua, Al-Slwhhaz s.n. (HN(]). ISI\ \|-'E. (dlhiia rnoiiiitain. 

Duns 1668 (E). JOKDA^. Jordan M.E.D.P. S/l! 13 (K). 
PAKISTAN. Chiiial, Tirieh, Siainlon 2780 (E). SAUDI 
AinniA. Rimiaii. White 73 (Kj. ^ K.MEN. Ilulh. l//7/rv- 
3156 (E): Sanaa. MtUer 3401 (E). 

iUl. Cappari^> siciila Veil I. subs{). iiies<>polamica 

Inoccncio. D. Rivera, Obon & Alcaraz. sul)sp. 

nov. TYPi:: [Iraq] ^'Vmara. 9 Se^). 1018, W. 
Edgar luans^ M/IOO (E)" (holoty[)e, designated 
here, hA, spccInH-n E 63908). Eigure 7. 

fndiiriicnliirn I tiflinrnatihiis lircv iorilnis, lOO-^T^O pm 

(Aipparis spifiosa L. xav. puhe.sccns '/.oh ii\-y\ Hull. Hes. Council loiigis. ct teniuoiihus. t3-2() pni lalis. inlcrnodiis acuh^s 

Israel (>I3: 56, 1060. TYPE: [Egypt] (Jaiala. rueks, a<l hasini trnnintihn^. 0.1-0.2 (-[ii. iH'(liceli.s hif\ iorilms. 3- 

■1100 ft., 1011^ P. JL Paris 8062 (hoi.. I) p.'. K[). 

1.3 cm. a t\ po dillcit. 

Volume 93, Number 1 

Inocencio et al. 

Revision of Capparis Sect. Capparis 



10 cm 

11. -7 

HfMails of llic new suhspeoies Capparis siciila siibsp. mesopatamica Tnoceiicio, D. Ri\('ra, Olton. & Alcaraz. 
■A. Stem and flower. — R. Detail of leaf and stipult^s. (A. R drawn by J. -A. Karrena fruui Furse 9021, K.) 

Slinil) j)rocunil)eiil: Ivvigs slialglit, up lo 2 in loii*^;, deep; slanieiis 100 io 150, anthers 2-2.5 mm, with 
ycHowish green; inlcrnodes 0.5-3.5 cm; slij)iiles aeutc apices. Fruit oblong, pulp red; ripe seeds brown, 
curved, relrorse, nol deeurrenl, yellow-orang^^ 0.2- 2.8-3 X 2. 1-2.o X 1.7-2 nun. 

0.4 cm long. 0.1-0.2 cm wide at the l)ase. Leaves 

obovate or oblong, 2.2-3.5 X 1.3-2.5 em, berba- f.ont of the lill(^ page). 

flluslraUons. Townsend & Guest (1980: pi. in 

ceous; iiuhunent very lax, triehomes thin and sliort. 

iOO-250 X 15-20 j^lni; leaf veins prominent; base September, 
acute, apices acute oi rounded; muero long, 1- 

Plicnology. Flowering and fruiting from July to 

Dislrihiilion and hahiiat. b-ano-Tumnian Region. 

Med i tt^rranean and 

Extending soiutnvliat into the 

Sabaro-Arabian Regions. Middle Fast [Iran, Iraq, 

1.5 mm, straight; ]>elioles sbort, 0.5-0.7 cm. Flower 

buds rounded or slighMy acule; floral pedicels slender 

and short, 3-4.5 cm; (lowers zygoniorphic; abaxial Israel, Syria]. Sandstone, often near orchards and 

(odd) sepal galeate, 1.2-1.8 cm long, 0.6-0.8 cm groves, at clevalions from lo 2300 m. 


Annals of the 

Missouri Botanical Garden 

10 cm 

^A a£ '(?i 




2 cm 



5 cm 


JA fiCdJ. 

Figure 8. ilrhiiU n\' llic new siil>sprcics (](!j)p(U'is siciiln Will. 

A ^ 

cni am 

>ii[)sp. sindiaiKi TiUK't'iiciti, I). Iii\(ua, ()l)()ii <*( Mcaraz. 
ower. —]]. Drlaii of leaf ami stijiules. ^C IViiil. ( \-C. <lra\\ii l>_\ J.- V. l^irn'M.i fVon! lAiUuau 92. K.) 

Parafyprs. liiA.N. (wilrslaiu Fnrsc <M)2I (K); Masjcd^-- 
Salcyinan, Lee ()H (K); Ma/aii<l('raii, Tt^lifaiu s.n. JOS-iO {V.). 
WWi). Aniaca. lulgur /■Jdiis M/U)i> (E); Saadisa. AI-Kaisi 
■12894 (K): Si.k. Gannalh R. Whrrlcr :i22 (R). ISKAKI.. 

MI/*I<' Dra-ol, l)('a(I Sea, Ih/nui c^' Kucvs 3-12 (11X0). SYWl \. 

Afii Dara. A'/Vr/v/ X- ()!>(>/! s.n. (ML Hj. 

He. Capparis sioiila Vcill. suhsp. siinliaiia Inoceii- 

Caulihus \ irI(lt'S(rnlil)iis v(;l Iiitcls, Lriclioiiial ihiis lax is, 
peduiiriiii^ Ihnalilnis *;i"a('illiinis l)i('\ ior'ilius. a lypo 
(lillrit. Slijjtilis aurcis, aiilhcris niinulis a siihspccirs 
nirsnpotaniira (lifTrit. 

Slirub pirocLunhnit, almost ^lal}rou-s; twigs sli'aigliU 
soiiu^ljnies icachliig up lo ,'■{ iii long, light green i)v 

cio, I). Riveni. Ohoii ^^ Alcara/. siil)s]). iiov. yerhnvisli: iiilcrriodcs 1-3 cin; slipulc^s i-iir\(Ml 


TVPK: [\fghnnislaiij liamk. 20 Aug. 1986. Mr. 
lAiUmin, 92 (liololxpe, K!). Figure 8. 

Capparis ahorala i\ovl{'. Illinois IJoL liiiiiai. \ils. \ ol. 1: 73. 
1830. TVrF: [Iliina.lial Ptadt'sh, India "llal.. Ilan-o 

sonu'whal curx ed. retrurst.% oecasiouall) .-^preadiug. 
not (leeiiiTeiit In snineAvlial decurrent. ^rnlden \elln\v 


coniraslliig u itii llie twigs, 0. 1-0.4 eni l()n<^, 0.1- 


0.2 tan wide al llie hase. Leav(;s ohovale or elliptieal, 

Chatigul 111 Kuiiauui- [Kiniiaur. K[iiau[ir|" (t\pe nol 1-3.5 X I ~3 eni. Iierhaeeous: leaf veins prominent; 
■^*''''l)- ba.^e ronnded. apices aente; muero \ery small, 

Volume 93, Number 1 

Inocencio at al. 

Revision of Capparis Sect. Capparis 


0.1—0.5 mm, straight or slightly curved; petioles dark yellow, 0.3—0.6 cm long, 0.1—0.2 em wide nl llu^ 
short, 0.3-1 cm. Flower buds acute; floral [)edlcels base. Leaves ovate or obovate, 4-5 X 2.5-3.5 ciu, 
slender, short, 1.5-^1- em; flowers zygomorphie; herbaceous; indumeut very lax, triehomes tliick and 

abaxial (odd) sepal galeale, 0.8—1.2 cm h)ug. 0.4 

long, 25-10 X 300-500 jam, early falling; leaf veins 

2 mm. 

0.6 cm deep; stamens 100 to 150. anthers 1.6-2 mm, not prominent; base rounded or somewhat tapering, 
with acute apices. Fniil elhpsoiflal to (ibh)ng, pulp apices aeule; muero very small, 0.1-0.5 mm, straight; 
red; ri[)e seeds dark brown, 2.8-2.6 X 2.4-2.6 X 1.8- petioles short, 0.7-1 cm. hlowei- buds acute; fli)ral 

pedicels thick and long, 5—6.5 cm; (lowers /ygoiuor- 
phic; abaxial (odd) sepal galeute, 1.8—2.4 em long, 
0.6-1.1 cm deep; stamens TOO to 150. anthers 2.5— 
2.8 mm, with acute a])ices. Fruit oblong, pulp red; 
ripe seeds brown. 3—3.2 X 2.6-2.8 X 2—2.5 mm. 

Illustrations. Royle (1839: 73); Nar^ i & Ali 
(1973: 8. fig. 2a); Polunin & Stainton (1981: [A. 16, 
n. 161). 

Plicnology. Flowering (jom July lo SepttaubtM". 

Dislrihiition and hahUaL Sudauo-ZamlnvJan, Indian 
and liauo-Turanlan Regions. Middle East into India 
[Afghanistan, bidia. Fakistaii]. Walls, meadows, and 
human tlwellings; from 1000 to 3000 m. 

In die lower lelt-hand part of the shet4 with the 
hololvpe oi' Capparis sicula \ eill. subsp. si?uli(ma at K 
is a label willi llic following script: "FLORA OF 

llluslralions. Coste (1900: 142); Woodville (1794: 
plale 228, drawn and engraved by James Sowerby). 
Phenology. Flowering from Ma}^ to October. 
Disiril)niion and habitat. Mt^dilerranean Reiiion. 

Mediterranean Europe, Mi 

( ( le 

Fast into Turkey 

[France, Greece, Italy, Spain, Turkey]. Cultivated, 

A ivMT \ MTCT^ \ AT Mo oo /M r ' ' T / soiu(^tinH*s fouud in set'ondary habitats as a feral or 

Ar(/I lAINtbl AiN IN . v2 / IName. L(ij)p(iris sj)inosa I,. / -^ 

Nati\c Name: Barak: dry riverbed, shale / Locality & 

Altitude: / surmy widespread growth, straggling. / 
Notes: proeimibeut stems. Fruit "wIkmi iipe / delnsces 
along 3 lines to ojx^n out as / mass of bright red slickv 

living among the parental species, al elevations Irom 

lo 2:')() m. Figure 2. 


N'cra et 


d tl 

10 status aiK 


UH seec 

Is / 


tvpilicaliou of Capparis spinasa. In summary, mor- 
bedded In latter / alt. 1430 m. / phol(»glcal, reproductive, and molecular data suggest, 

Collector: Mr Lulman / Date: 26.8.1968." 

The John Forbes Royle Herbarium is at LIV; 
how^ever, Donna Young (pers. comm.) has checked in 

bul do not prove, that this is a h)brid species kejit in 
enhivalion. Fhe origins of ihe different populations 
are related to the coincidtMiee of wild and/or 

the Roylean herbarium and verified that no type cultivaled individuals in proximity, belonging lo C. 
sp(H'imen for Capparis ovala is there. Other herbaria ■^'^''^'^^^ ^»'"1 C. oricntalis, especially in the Western 
where i)ossible original material may be (DD and K) Mediterranean [Sicily, Mallorca], but also in Greece. 
were unsuccessfullv eonlacted. Therefore a n(M)|vpe is The diversity within this crop shows a pattern of 

variation Inlermediale b('lw(M'n tlu^ putative parentage 


raratypes. Ah(;i I AINLS'LAN. Barak, Ldnuai 92 (K). 
tNDlA. WangtLi to Sliollu, Cluillo bridge, tjaslialii", PLiiijal), 
Lace I7H (Kj; Li, tUislialif. Simla. Eastern I'lnijalt. I^iinuti- 
mnitl 725 (E). PAKISTAN. HmIii. l>kalkoo. W mlcrhoUoni s.n. 

(Kivcia el al., 1999). 

Sri eel ('(I sj)ccin)ens exawinrfj. h'RANCE. MoalprlliiM-, 
Befidunn 213 (F); s.l. Ap;ardli. s.n. {{.). GllEECE. Illiodcs, 

(K); Caiul nullah. Cnpis, Cilj^il. Karaclu, Omcr 266 (E); Saadamaun s.n. (C); PitIuI Bulaiiiral Garden (unknoun). 

Cili:;Il-Kariinal)ad- loOOin, Qtdscr, Omcr & llusdiii nI44 
(KiN(;); Kharipur, J<dri 2421 (E); Shanlu. Hatli^lan, ,S7;./// 
249 (E); above the liidiis I'iver, Slianlu, Kasliniii-, liallislan, 
2r){)()in, Webster & Nasa 5771 (K). 

Jjisfcn s.n, (C). tTALY. Sicily, Agri<;;ento, Denis 40229 
(RN(;); SUoiuholi, B. Larscn s.n. (C). SPAtN. Alicaiih-: Kl 
Caiiipeilo, Inocenrio & Alrarnz s.n. (MIIH); i-^araiso Reach, 
Villaioyosa, Uewin H 1040 (11N(]). Barcelona: Barceloiui, 
Sennen 1587 (RNG). Corilolia: I'- 1 TeiapkHe, C. Ldpfz 
€14971/86 (RNC). Mallorea: Ranyalbufar, Inocencio & 

9. Capparis spinosa L.. S|). pL: 503. 1 i53. d^VLL: Maudz s.n. (MLBJ: Canipanel Cav.^s, Inocencio & Meardz 
[France?] "Habital in Europae australis arenosis. ^■"- (^';^^^)^ f;'";; 1^^"'^ ^^^;^»^ ^"'^\^!:^™ fl.i';'!'^^ 
ruderatis" (leclotype, designated by Riirtt & 

Lewis in Kew BnlL 4: 299. 1949, HM, Herb. 
Clifford: 20:5!, Capparis No. 912.;5'1P)-S(), vali- 
dated by Jacobs, Bluniea 12/3: 417. 1965). 

C<!pp<nis j)eduncidoris Presl., I)(^lic. Prag.: 20-21. lo22. 

Shrub ])rocnnibent; twigs straight, sometimes reach- 
ing up to 3 m. dark green; internodes 1.5-3.5 cm; 
stijiules curved, retrorse. not deeurrent, slernler, weak 
or vestigial, rarely strong, usually very long and thin. 

s.n. (MIR): \ alldemosa, Chrisfensen 1372 (C). TURKEY. 
l)eni/[I, lUinel 00.437 (E); Eskiscliir-SiiiKliluai, Eliini 373 

10. Capparis zoharvi FncxH^neio, D. Rivera, Obon 
& Alcaiaz, sp. nov. T^ IMi!: [S[)ain] "El Llano del 
Beal, Murcia, Spain, 7 Jul) 1999, Inocencio 
426lVr (holotype, designated here, UMIll; para- 
types, Inocencio & Alcaraz 70102, 70103,48689, 
s(^nt lo K, E, and MO!). Figure 9. 


Annals of the 

Missouri Botanical Garden 

1 mm 


3 cm 

6 cm 



1 CIJ} 


Figure M. Octails of tin' new s[)<'rtrs Capparis znluiryi irHKciicio, I), luvcnu <)\n)\\ & Alrara/. — A. Ilahil. — H. Detail ol 
leaf \ aiiahility. — C. Sletns. — V). Dt-lail ■►(' the stipules, — \]. Detail of iieelan'. — V. Detail of anther. — C. Fruit. ( A-(; (h-awn 
Ity P. Perales ^K J, -A. Rarrena from Inocencio & Mcuraz 1H6H9) 

Volume 93, Number 1 

nocencio et al. 

Revision of Capparis Sect. Capparis 


Fruti('(^s (M'(H'li, iisf[ii(' ad 2 m; stipiilis [Irrunriililuis, 
siniilihiis rosaris: folils roliindis— ohc-orclalis. raiiiis (>\ali.s, (2— 
4 cni loiigis, 2 — l cm lalis). apice eniar^inati.s u-1 nhuisis 
a C(}ppar'is aegyplla dilfrrl. In inenioriani Mi(hac-li> /ohan 

Shrid) erect, glabrous; twigs straighu ± creel, up lo 
2 ni l<»ng, green to reddish purple, older Ivvigs l)luish 

at the rank of variety or suhspecies hav^e been here 
recogtd/ed as species or subspecies. One ol Uie 
reasons for ihe syntheti<:' approacdi of Jacobs ({Qf).")) or 
Zohary (I960) is the relaliw fr(H|ucncy of intermedi- 
ate in(li\i(hials in he!l)ariuin specimens ihal ol>scure 
the clear distinction among species. We refer to most 
of these as hybrid indivi(hials, as revealed by our 

due to a waxy covering; iulernodes 1-5 cm; stipules Heldwork in the Iberian Peninsula and Norlli Africa 

curved, retrorse, strongly decurrent, rose type, orange, 
0..'5-0.6 cm long. 0.3-().d' cm wide at the base. Leaves 
rounded to obcordate, rarelv ovale. 2—1 X 2—4 cm. 
some\\haL fleshy; leaf veins not proniiueni; base 
rounded, sometimes coidale, apices rouud(Ml or 
slightly obcordale; mucro absent or very small, O.I- 
0.5 mm; petioles short, 0.7-1 cm. Flovv<u- buds 
rounded; floral pedic(ds thick and long, .3-5 cm; 
flowers slightlv zvgomorphic: a])axial (odd) sepal 

(Lioceneio, 2001). 

Hxbrids have been reported from diflerent areas 
in which presumably hybrid swarms occur between 
two (hllerent Capparis species growing togclluM'. 
Ibbrids aic freqnent in Iracj and neighboring 
countries of the Near Kasl (Hlakidock & Townsend, 
]9u0), shadowing the (list I notion between species. 
The most relevant interspecific hybrid, for its 
econotnic uses, is C spinosa^ which is also ihc l\pe 

slightly galeate, 1.5-1.7 cm long, 0.6-0.0 cm ^Irrp: "^p^,.;,.^- ^^f ^i^^ genns. It occurs spontaneously in 

stamens 30 to 80. anthers 1.3-1.5 nun. with I'ctuud 

populalious of C, orieniaUs growing close to those 

apices. Fruit oblong, pulp yellow- ripe seeds brown, ^^p ^; ^-^.^^j^^ j,^ t|^^ western Mediterranean (ln()C(^ncio. 
3.4-3.8 X 3-3.2 X 2-2.2 mm. 2001). Otdy this nothotaxoii has been widtdy taken 

lllustnilions. Figure 11 in Zohary (1966: 358). 


Flowerinii: and Iruiting fntm Mandi to 



Distrihiition and h a hi I aL Mediterranean Region. 
Mediterranean Eun)p(% North Africa, Middle Fasl into 
Turkey [Algeria, Egypt, (^reece, Israel, Jonkm. Lebanon, 
Morocco, Spain, Syria, Turkey]. Walls, rocks, 
pronounced slopes, al elevations from to 200 m. 

the Algerian type 


often ill the vicinity of liuman dwellings. Hgure 4. 

Pamfvpes. AkCKHtV. Cliiffa, Blida, Daris 59527 

(F). VX'AVT. S.I., A^. Tadmor cK: A. Shmula S-42() (K); Sinai, 

note 273 (K). Gl^d^l^(d^. Samus, W, BarU-y 653 (I-]). 
SI'AIN. [Vlurfia: Kl klano del \U"d\, Alcaraz, li'nrni cK: Ohon 

48755 (MUB). TSR A !■:!.. Fin CrrVu 0. B. Lysche<h' 9/99/71 
{{]): Kfar Gileh v MiUKu-a. Curie 65 (K); Manara, C. M. Curie 
145 (F); ^h)unt Gillma, Dails 1667 (E); Wadi i}v[[. Daris 
3651 (E); W\idi Yannnk. DuiLs 1604 (F). JOKDAN. Sonlh 
of Rum Rest House, Jalidd et al 7636 (F); Vi'adi 
Mujil^ Ma'tkiba, L Houlos 5356 (K). FFRAiNON. Heirnl. 
s.n. {K). MOROCCO. Safi. 20 June 1999. hunvnclo 60025 
(MUK). SYRIA, Am tiara, Rirera & Oln'm 60019 (MUt3); 
D^nuLscus, Rirera cK: ()h5u 60018 (MUB); Maaral»a, Rlrcra 
cK: Ohi'm 60046 (MUB); t\dni)Ta, Rirera & OI>5u 60051 
(MFB); Ugarit. Rirera ct" Oln'm 60045 (Ml'B). TLRKFY. 
Adana. E. K. Balls IJO iK); Manya. Bayh>p ')70i (F): 
Anlalsa. Smith 4 (K). 

ifilo cuhixatioii. There have been no reported iu- 
lerscclioual hybrids within Capparis subgenus Cap- 
paris. although Capparis oraUi subsp. luyrti folia 
seems to be an intcrmedialc between C. ovata subsp. 
orala and C. ifieruiis and, therefore, presumably 
th(Mr h)bridogen. Capparis orala is here reslricled to 

and those poitidations clos(d 
related in mo]-[ihology dial extend from Morocco to 


The large complex of Ab-ditciranean and Irano- 
Turanian taxa formerly subordinaled to Capjxiris 
spinosa is here combined imdcr C sicula because 
this is the name available according lo the principle of 

iJU'iatntc CAwd 

AM, S. cK S. Jah'i. 1977. Cappararrae. P]). 1-20 /;/ S. Jahi (X 
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Anonvinou.s. 2(){)S, CBD Slrulegv and At lion Plan — Tajiki- 


This paper introduces changes in the C<ipj>aris sect. 
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(1960). who organized the (h\ersitv within this section 
around two core species, \ iz. Capparis spinosa and C. 
ovala. Musi of the endemic taxa that previously were 
suboi'diuated to one or ihe other of the al)ove species 

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Rivera. D.. f' . \lcaraz. C. Inoeeneio. (1. Oh(')n t^ 1-7 (^uifalo. 
1999. Taxonomic slud\ of (ndlivalod (^.apparls seel. 
(Capparis in the wesleru Modiloriauean. Pp. d'5[— 4-55 in 
S. Andrews, A. C. [vosjie & (7 .Me.xandci' (editors). 
Taxonomy nf failti\ated Plants: Third International 
S\niposiuni. Ho\al B(>tanie (hardens. Krw. 

. C. luoc(aieio. (7 OlxMi, 1'7 Faireno, A. Beales tK V. 

Alcaraz. 2002. Aichaenhntarn' of capers [Cuppa ris) 
((!ap[)araceao). W^g. lli>l. \reliaeo|)ol. 11: 295-313. 

, E I'^riis, C. Inoectaao. (7 OFiin. E. Ah-ara/. v*^ A. 

Ileales. 2(103a. The I) pif Icatiun of Capptiris incnnis 
I'orssk.. 6". sinaica \'eilF anrl 6'. cnrfilai^incd Doene. 

((^apparaceae). 'Faxon 52: 307-31 1. 

. C. [noooncio. 0. Ohi'm t^' I^". Aleara/. 20O.")h. I\e\ iow 

of Food and Medicinal I ses o( Capparis F. suh^onns 

Capparis ((7i[»paiidaeeae). Econ. Bx't. 57: 5F5-5.')F 

, , , \. Keah's \!^ E. Alcaia/. 2()()(>. 

(Capparis sjtinosa F. (Ca|)[)ai'aeeae): TIk^ ap]4icalion 
ol the nauH' after studv ol llio lectol\ [)e and t\pifi- 
calion of 6'. simla \ oilF and C, nricnfalis \ eill. 'Faxon, (in 

Kodinau, J. F7, P. S. Sollis, 1). E. Solti>. I\. J. S^tsnia c^ K. C. 



f gluco.sino 




u-o[. ivvc). I arallel e\(j|ntion o 
s\ri thesis u if erred fi'orn eonirrneni nuclear and plastid 

<^faie phslogonios. .Anu-r. .1. Bot. 85: 997-1 OOC). 
Rovle. J. F. 18.39. III. hot. Mitnal. Mis.. Vol. F W. H. Allen, 


, E. Alearaz, E. Calderon. (7 Ohon 1.K D. Kiv(a-a. 2002. Smillu J. E. 1825. Flora Oraoca, \'oF \7 Kichard Ia\loi 

Tht^ use ol lloial tdiaraettas in Capparis seel. Capparis to 
detorinine ihe holanieal aiul geographical oi'igin of eapcrs, 
Eur. Food Res. TeehnoF 211: 33.5-339. 
. R. Cowan, C. Piivera. F. \haraz, E. Eav & M. 2005. 


St alien, V. kS R. S. f 'owan. 1976. Taxonoiuio Fiteralure. 


Vol. I: A-C. Regmun \Cg. 94: I- I \M). 
i^ . 19.9. Ia\(nioinie [aUaatui'e, \ ok IF II- 

AFFP fingerprinting in Capparis L. snltgtanis Capparis 
((7ipparaceae) related lo the eotuiuorcial sonre(\s ol capei's. 
(ronet. Resouices iK ( 'rop E\()F 52: 137-144. 

Fe. Regnnm Veg. 98: 1-991. 



. 198 E FaxoiuMnie Filcialun', \7)l. Ill: 

Fh-O. Ih'guuin Veg. 105: 1-980. 

Volume 93, Number 1 

Inocencio et al. 

Revision of Capparis Sect. Capparis 



. WiYA. Taxoiiomic LiU■ralu.(^ Vol. IV: P- Valdes, 15., S. Talavcra & E. Frrnainh'/. 1987. Fl. 

Snk. Ke^jnuni Ve^. IK): 1-1214. 



. 19IJ3. Taxonomif Litcratinf, Vdl. \ : Sal- 

Sir. Rc-iuim VeK. 1 \2: 1-1066. 


. 1088. Taxononiic I.iU'raliirr. \()1. \ TI: 

W-Z. Kegnum Veg. 116: 1-653. 
Tackholin, V. 1974. StudciiLs" Fl. Egypl. Cain. Ftiivrrsily, 


Taklilajan, A. 1966. Flora AitiK-nii. Vol. V. Aka.lriiiii Nauk 

Arniiatiskoj SSR. Frc\an. 
. 1986. Floristic RcLMons of [he Vi\>iKl. Liiiv. 

Caliioniia Press, Rcikclcv. 
TouiiseiKl. C. C. (l^l F. Cuest. 1980. Fl. Irati- \ nl. I\llj. 
Miiii>try of Agriculliirc and Agrarian Roforni. naghdad. 

Orcidcntal. Vol. 1. Kctres, Harccloiia. 
\avilov, N. F 1931. Liiiiiacus species as a syslein. Trudy 

Prikl. Bol. Genet. Seleke. (Bull. ai)|)F Bot. Gen. PL 

Breed.) 26(3): 109-131 
\X'illis, J. G. 1988. A Dietionarv of the Flowering I*lanls and 

Ferns. Figlilii Fdilion. Caiubridge Univ. Press, Cambridge. 
Woodville, W. 1794. Medical Bolany. James Phillips, 

Zohary, M. 1960. The species of Capparis in the Mediter- 
ranean and die Near Eastern Countries. Bull. Res. Conned 

Isra(d. 81): 29-64. 
. 1966. Fl. Palaestlna. Vol. F Plates. The l-^raeli 

Acadcui) of Sciences and Humanities, Jerusalem. 

THE CARDUEAE (COMl^OSITAE) ^^'f'»^'<> Susanna,' Nmia Carria-Jaras,' Oriane 


ITS, //7iL-/r/zF, AND malK 




Hiddlgo/ Rose/ Vllatersdna;^ and Teresa 



()i(M)\r|-. rif'W 

Thr lieu ..iitlinr of relationships m ha.sal l.ranclics of lli,- (arriil) Coniposllar Cisrkc cotirintis ihal tlir sislrr -roup lo the 
triho Car.lurar Cass, an^ not Mulisi,>ac Cass., hul rallicr a ^roup of Alrican -cnrra now Hassificil as llu^ irihe Tarrliotianthrae 
Koslel. This change implies ihal ihe nionoph)!) n{' t!ir Cardueae iniisl be reassessed on a inolernlar basis. M 
eoJIeellons in irrrui wars allow ns lo extend oiw samplin- to 70 of l[,e 74 gen^M'u ni the trilje. We perfumed a nr^^ moleeular 
stLKly ol the trdje UMng on,- nuclear region (ITS) an. I two ehloroplaslie niarkrrs [Irnl.-lrnF and malK) in addili..n \u a more 
approprn.le outgmup. Our resulls confirm thai [he Carducac i^ a natural group bnl indieaK' sotne changes in sulnribal 
dehnealion: the subtri[)e rard..|Mtiinae Less, is recognized and some genera are move<l to other sul, tribes (Mynpnn/on lioiss., 
Nikillmu lljin, Syreiischihoria Pavlov, and tlie Xeranlhrwuin L group). A reeapilulalion of a number of inlcn-sling (|uestions 
that remain unresolved in the classification of some largi^ geruM-a is prcsent<^d. 

Kry words: Cardueae, Composita.-. genus d(din,^ation. ITS. mnlK. phylogcny. tribal delimitation, tm\.-lniY. 



nuevo es(|uema de las rclaeiunes en las basah's de la lamilia (:omposita<- Ciseke lia conbrmado (inc el -a 



liermano de la Iribu Canhieae Cass, no cs la tribu Mutisieae Cass., sino mas bien un grnpo de gen(M-os africanos .pi.^ ahora se 
dastlican eomo Iribu Tarchonanlheae Kos|.-|. K.sie c'ambio impbea (jue la monofilia de las Cardueae eslablecida .obre bases 
moleeulares dcbe eonfirmarse. Ademas. miestras nuevas reeoif^eeiones en lor. lillunos anos ha.-cn c,ue nuesiro murstrco se 
exlicnda a -0 de los /4 genero. de la Inbu. Memos llevado a cabo un nuevo esludio molecular de la Irilni usaudo una region 
nuclear (ITS) y dos cloroplaslieas. ademas de seleeeionar un grupo .^xterno mas adecuado. Nueslros resultados conbrMian'^iue 
las Cardu.Me son nn grnpo nalurab per., aeonsejan algunos cainbios en la delimitacion subtribai: el reeonocimienio de la 
snblnl)u(:ardopaliina<" Less, y el eambio d.> algunos gen(a-os a oLras subtribus [Myoinmlon Hoiss., NiLifinia lljin, 
S)rcilsrlnLon<! Pavlov y el gnip.j Xernnfhrmiini L.). I^vsenlainos lambien una recapit'nlaeion sobre eierlas cuestiones 
intere.-.antcs (pie que^hni sin resolver en hi clasifieacion de ahuuios irrandes -eneros. 


a cdassiliealioii of Iwo suhfainilies and 16 tribes that 

()\Eii\llA\ OK (:()\1IM)<IT\E SYSTKMATICS 

a i lied 

gaiiiea geiKMal acceptance initii ven 

it'ceiilly. The 


two latest revisions of the fatnilv, toward ihe end of tl 
The s)sli^nialics of Coinpositae is niarke<l by thrxM^ 20fli centiiiy (DiHrieh, 1977; IJreiner, 1991), lollowed 
jnllestones. catdi one itividving dcM^p (dianges in the llofrniann\s (dassificalion. The ibird sol of lar-c-scalc 
classdic-alion ol the fainil). Since the lnsU)ty ol' this changes was produced by the [[Mrodnction of methods 
classilicalion has been re\ised in depdi in bnnk et ah l)ased on DNA analysis. First came the pioneering 
(2005), here we give oiil\ a shoi1 summary. Tlie fir.^t stud) by .h 

niscii <M Palmcj (1987) using cpDNA 


attempt to classify Composilac was made by Cassini reslriction site [lol} morj)hisms, which led to d 
(1819), who defined 20 tribes. A more synthetic description of a third suhfannlv. Barnadcsloldeae 
system was proposed by nenlham (187;5) and, soon (Bcnlli. .^ Hook, f.) K. Hremer & K. K. Jaiisen; ibis 

after, I lolTinann (189 1). Both authors proposed 

j)ro])osal was ivflecTcHl in Bremer (1991). Second, the 

' Financial supf^orl from the I)irecci6n (icncral .k- Fiisefian/.a Superior. Spain { IVojcel PH 97/1 \'M) Ministerio dc ( i.Micii y 
Teenologia. Spain (Projecr. Pli IU)S2()()1 -;5() 1 1 -C()2-02 PII IU)S2002-lin.V,-K) ami Generalilal de Catahuua {-\|uts 
agrupsdereeen...MH.soli(]al>"1999S(;i{()();i'^2au(12()()lS(;iI(Kll23)isgra^ acTnouledged. Wc thank ChriMJnc rildab-o 

for her help m .se.juencuig tlu- !rn].-!rnF region aiul Mirpid Venv for keeping the colhM-tions of living plants. Wc al..o ihank 
Sanlia-o Orti/. L niversitx of Santiago, Spain, uho provided material and serpicn.-es of Bmrlnlama. Ohlrnlmr'na and 

,,//,,■>■ Tl 11. ,1 .: r.c^ 1 , ■ I T I- . 1 ■..,,. ^ - , , . . . ■ iD > 

Tdfrhonanlhiis. The cojhiboiation .)f the bolanical garden^ li>tcd in Table 2 is als(» ack 


f(>r- ihcir \aluable suggeslions lor Improving the manuxript. 

\i^ ihi; 

now le(lgc( 

. W c thank \ iekl l''uiik and 

one aii(Hi)mous revunvej' lor In 

-The etiilors of llic Aniuils ihank Sophia Ualcomb for her editorial eoiH rlbul u)n le mis paper. 

■^Botanic Institute of Barcelona (CSlC-Ajnulanu-nt de IJareelona). Pg. del iMigdia s. n.. K-Oimil liair.dona. Spain. 
asusannaO' ibi). 

Ann. Missorni IJor. Card. 93: 130-171. I\ihi,isiii-;i) on .31 M\^ 2006. 

Volume 93, Number 1 

Susanna et al. 
Cardueae (Compositae) 


'ral)l(' 1. Oiillinr of \wo diffrreiil projxisals of classificatinn of C(>rnf)()silac (oiil) basal hraiichcs). 

BIlEMKIl (1994) 

UAHNAOESIOIDKAE (Bmtli. & ITuok. f.) 

K. Bremrr & R. K. Jansrn 





. VER\OMEAE Cass. 
. MVBEAE Rvdh. 



(3 sulifaniilios. 17 Irihcs) 

PANERO .K EUNK (2002) 

BABNADESIOIDEAE (Bcnlh. & Hook, f.) K. Bivhum- cK^ R. K 



Slirrii(M(lcac cladc ([irov isidtial) 

• Sumieae rladc (pn.vlsioiia!) (S. AMERICA. AI'BICA) 

METISIOIDEAE (Cass.) Eitull. 

. MlTiSlKAE Cass. (S. AMEI{1C\ 

(;()C11^ATI0II)EAE (B.-nlh. iK Hook, f.) Pancro (.^ V. A. Eunk 
11ECAS'D)CEK1D()IDEAE Panero i^' V. A. Eunk 

• HECASTOCkElDEAE Pan.-ro K- V. A. Punk 
CAPvDEOIDEAE Cass. e\ Swocf 

. DK:0MEAE PaiuTu & W A. Eunk 

.T\ilCnO.NA\TIlEAE Ko.Lcl. 
.CV1!I)LE.\E Cass. 

(11 sultfainilirs, 36 Lribcs) 

latest and more i-rvnlutionaiy s[udyl)y Dancm&- Cutik (2()(12j. tribe Cieborieae {Tragajn^gon) Is derived in 
(2(K)2j analyzed sequences of nine eldoroplast regions ndatioii to Canbieae; Ainsliaca and Warionia do not 
across tbe entire family and proposed a new classi- b(don- to Alutisieae l)Ut lo Pertyeae Panero & V. A. 
fieation wilb 11 sul)farnilies and 3;1 tri1)es; tbis was In Funk and Cnndelieae IL Pvol). S^ Bretlell, respective- 
some ways closer lo Cas.ini^s analytical views iban to h% botb Iribes also derived uitb regard to Cardueae; 
tbetic annroacdies. ddie dramatic diffcRMices b(- and Ccrbcra and MuUsIa are pbiced in Mulisieae 


tueen Bremer's (1994) and Panero and Funk^s (2002) sensu siricto, pliylogeiu'tically far from Cardueae 

cb-issification are iliustraled in Tabic l((mlylliel)asal (dable 1). With these outgroup species. Cardueae 

groups are sliown). Tbe high statistical support for die will always be monopbvletic, and mouoidiyly of ibe 

latter and its sound correlation with rtiorpbology leads tribe has always been a conlroverslal issue. Tbe 

us to bfdieve tbat \hc new classification of Composilae outgroup should be cIios(M1 from tbe cladc formed by 

tribe Tarcbonautbeae [ilus ibc genus Oldcithurgla L., 
lade tbal appears as the true sister group to 

is near to being definitive. 

a c 


Canhieae witb bootslraf) su|)[)oia values oi 100% m 
Panero and Funk (2(>()2). bi fact, Cardueae, Dicomeae 
Cardueae Cass, is one of the largest tribes o( I'anero & V. A. Funk, and Tarclu)nautbeae (i)lus 
Compositae, witb ca. 2500 species. Previous studi(^s Oldcnlnirgla) compose a monopb\b^tic subfaiuily, 
based on DNA seciuence analyses, bodi nuclear Carduoideae Cass, ex Sweet, also wilb tbe Ingbest 
(Susanna et al., 1995) and com1)ined cbloroidasi and statistical sup|)or[ (Panero & Funk, 2002). Morpbo- 
nnclear (Garcla-Jacas et al., 2002), confirm Caixlucae logical] cunnections between Caj-dueae and the rest of 
as monopbyletic. However, tbe new ilassilicalion subfamily Carduoideae are, ho\vevt!r, unknown to dale;. 

sliows tbat our previous oulgrouj) cboice was not the 
best cboice. In ibe classic system of {]omi>ositae (e.g., 
Eleywood et ab, 1977; liremcr, 199 1), Cardueae were 
classified in subfanuly Cichoiioidcac Cbevalb, close 

■ruiBAr ri^rrs or cakuufar 

In llie earliest classification (Cassini, 1819), 

to tribes Cieborieae Lam. & DC. and Mulisieae Cass. present Cardueae were divided in three Iribes: 

(Table 1). Tberefore, in our flrsl nucleard3NA-based 
phylogeny (Susanna el ab, 199.5), die outgroup was 


1 of 


Fcbinopea(% Carbtiea(% and Cardueae, ibe lattt'r witb 
two subuibes: Carduinae and Centaureinae. Rentbam 
(1873) and Ilonmaiui (1894) proposed grouinng ibe 
three tiibes in a single tribe Cardueae ibat beld four 

Cieborieae {Tragopogon E.) and 

three Mutisieae {Ainsliacd DC, Ccrbcra E., and 

Warionia Bcnib. & Coss.). In Carcia-Jacas el al. subtribes: Fclunopinae (Cass.) DumorL, Carbninae 

(2002), we replaced Ainsliaca, Tragopogon. and (Cass.) DumorE, Carduina<> Cass., and Centaureinae 

Warionia because of tbe increasing difficulties in (Cass.) DumorE Tbis w^as a conservative approacb tbat 

Mutisieae as was generall) accei)tcd for a ver\ long lime. However, 

discussion on tbe status of Fcbinopinae restarted 



aiii^ning tbe 11^ region, anil we used iwo 


I t 

out groups, 


)cra aru 

1 Mutisia F. f. However, 

according to die new cdassiHcation by Panero ^ Funk wben Viagenil/ (19.6) proposed die segregation of tbe 


Annals of the 

Missouri Botanical Garden 

siihtrihc as a separate Irihe, Eeliiiiopeae. Dillrieh 
(1977) reliinied lo Cassini's fail) views and proposed 
the restoratinii of Kehinopeae and Carlinea<^ Kiiially, 
Bremer (1991) reintrodiieed llie conservative ap- 
IHoaeh witli only one trihe, (^ardneae, wliieli, accord- 
ing to OLH- Jiiolecular studies, is a belter soliilion 
(Susanna <[ al.. 1995: Careia-Jaeas et al., 2002). 

In Careia-Jacas el al. (2002) we suggested Uiat 
n]a}l)c a fifth suhtrihe could he recognized. Cardopa- 
tiinae Less.- with two genera: CfirrlnjKiliuin Juss. and 
C()usnii()j)S!s Nevski. Cardopatiiuae were placed in an 
iiitertncdiate position h(4\vecri Carlininac and the res! 
of iho trihe (Garcia-Jacas et ah. 2002). I however, we 
hav(^ postponed th(^ resloratiou of this snhtrihe until 
mor(^ uuanihignous e\ idence has been collect(Ml. 


Withm Cardueae, there is g(aieral agrtuancnl in 
accepting four groups, regardless (if ihe rank (trihe or 
snbtribe) adopted. Three suhtiibes are natural (C:irli- 

Gi-:Nt:in(: limits in ri;ii5K cakdikai^ 

Other points of interest arc genus affinities and 
htnils in Cardueae, a Irihe with sonic of the largest 

ninae, Echinopinae. and Cenlaurcinae) and the fourth genera of the family. R(-arding genus affinities on 
(Larduinac) is a paraphyh^lic assemblage {Ci 
Jacas el ah, 2002). 


tlie ])asis of niorpliology and partial mohnailar studies, 
ihc two hn-gest snbtribes (Carduinae and (^enlaurei- 

Subtribe Carlininae is sister lo ihe rest of ihe l,il)e. nae) were subdlNuhnl inK. informal groui.s (Susanna c^ 
A striking and prolmbly plcsiomorplnc charact(M- is Garcia-Jacas. in press), which should I 
the presence of true ray Htirets in at least one getms of against a more comprclieusi 


)r cliecKe( 



Carbiunae, Alrdclylis b., while remaninig suhtrihes 

ve tnouH-utar pli\log(ni\. 
As to genus limits, in oin- kilesi revision of (lanhieae 

have only disk florets, Capilula are usually subUmded (Susanna & Garcia-Jacas, in press) we adopted a broad 
by peclmate-pinnatisecl leaf-bke brads: corolla lobes generic concei)t h,r Couslnm Cass. (000 species), 

Jiirifira Cass. (200j, and Saussurea (100) bec-ause of 

are very short, onl\ 1-3 

nmi long: ano me paj)pu 


s Iia^ 


lono, plu.nose hrislles. often connate al llir base ,1,^. la<k of recent syslenialic revisions for all three. 
orming l.roa.ler, robust scales (Snsanna ^ (iarcia- RecenlK, 0,1 tlie basis of a partial sin.l) of DNA 

secjiienccs anil aciieni' niorpliology, Raab-Slanbe 
Sublribe Keliinopinae is easily characterized by its (2()();5) proposed Hie restoration of t 


Jacas. in pic^s). 

wo sin 




secona-or.lcr nntorescences (nnillowered c-a]).tnla Froluria (DC.) Lipsch. and Lipsclutziella Kan.elni. and 

clustered in a large synfloivsccnce). Olu" latest 
molecular ph) logon) intlic-al<\s that Eehinopinae 


desci-ibcd a new genifs. Himdhnelhi liaab-Staube, all 
of these within the Saussurea group. 




With the addition of 

new mat(M"!als, oin- DNA 

should also include the gen<'ra of the A'l 
group and w(^ jireviously |)roposed that tlu 
heads of the genus AVf//?///e///////? and allies could be 
interpreted as reduced synfha-cscences (Carcia-Jai-as 
et al, 2002). samj.ling covers 70 of the 74 accept(Ml g(Miera of 

Suhtribe Carduinae is a para|)hylctic complex of Cardueai': only AnnUliia DC. (Carduinae. Central 
genera wilh some well defined groups {Arcliuni b. Asia), Cciilannulendmn Johow (Cenlaurcinae, Juan 
gi-oup, Onoponliif)} b. group, Saussurea DC. gron[), or 
tlu^ ihisilcs) togclher wilh genera of prohleniatic 
ascriptictn like Berardia \ill. or Staeheliaa b. All 
ihc genera of Carduinae have basal or basal-abaxial 

Fernandez archipelago), (ronioeaulofi Cass. (Centaur- 
einae. India and East Tropical Africa), and Takei- 
kadzuehia Kitag. & Kitatn. (Carduinae, M 
absent. lh»ue\('r, the j)osition of lhes(^ within the tribe 

ontioiia are 

insertu)ti areole of aehenes and. usually, a simple and their snl}tribal ascription has n<^\ta- I 


pappus, and are oflen spiny. 

Fuially, snbtribe Centauj-elnac is the most derived 
group and is characterized bv aehenes with lateral- 


on a morphological basis (Snsanna & 

Garcia-Ja(^as, in press). Jo test our broad g(aierie 
concept, we includtMt th(^ genera Frolorla, LipsehU- 
adaxial insiniion areole, a double pappus, and. witli zielta. and Modestia Kharadze t^- Tamarnsch.. which 

few e\ce|>lions, unarmed heaves. However, examinin^i 
the bmils belween Carduinae and Centaureina 
r(^[)resents a challenge, because diffenaices 

we submerge in Juriaea; and Auiira (Knit.) J^seluM'- 
neva and Tiaroearpus \Ue\^. f., which we had 

K^ ni 

previously considered in (A)usinia (Susanna & 
mIcnxJiaraclers (»f the aclume and i>appus ihat are Garcia-Jacas, in pn^ss). We also inclnded the 

dilficailt to f}|)s(MTe in incomplete or immatiu'c 

published sequence of the recentiv desciibed 


herbarium materials. The examples of Nikiliiiia and Himataiella. For this wide rep^^seutation of Cardueae, 
Syreitsehikor'ui Ibustrate these difficailties (Susanna et we com()leted the ffS and uialK regions and. in view 
ab, 2002) and ihe ascription of these and otluM" genera 
should be checked against a molcfadar phylogeuy. 

of the low resolution of basal groups in previous 
analyses, we added a new marker, bow ri'sobition in 

Volume 93, Number 1 

Susanna et al. 
Cardueae (Compositae) 


iTiany molecular pliyloyenies may be solved by adding 283 lor a lotal of 466. The origin of ihe sam])les and 

more data to DNA se([uenee matrices as discussed ui dieir CeuBank accession numbers are given m 

Panero &" Funk (2002). We used a chlorojilast marker, Table 2. 

the IruL-trnV intergeiiic region, uliich is widely 

ulib/(Hl in Compositae (Bayer & Starr, 1998; Liu et una lATKACiiON. AMPLiiiCATiON, AM) SEniENCiNO 

ab, 2002; Oberprieb-r, 2002; Panero & Funk. 2002). 

Onr goals were to: 

(a) verify monophyly oC (^iinkkjac using spt'cics fnmi llie 

.sister cladc Tarchonantlu-ae and Oldcnbnrgui as an 

(I)) c'Uirify snblrihal rlassificalion and (Irfinc ihr posilion 

of Cardopaliinar. uhirli might consliUilc a liflh Mih- 

((•) examine whether lh(^ inlornial spccit-s groups defined 

in subtrihes Canhjinae and Ccntaureinae are naUn-ah 
and cheek the systematic posilion within lliese gronps 
of "eiiera not inehided in our previous sUidies: and 
(!) verify the suitahility of a inroad generic concept in 
(■(a-tain larg(^ genc-ra of Cardueae by anals/ing spi-eies 
from genera that we had previously rcjecled on die 
basis of morphologicnl characters. 

Total genomic 

DNA was extracted following the 

rtiiiiiprcp j)rocedure ol Doyle & Doyle (198i) as 
modin(Ml by Sollis et ab (1991) anrl Crdbngs (1992), 
from silica gel-dried leaves codected in the (i(dd or 
from fn^sh braves of pbmls cultivated in the Botanic 
Instil uic uf Barcelona. Tn some cases, herbarium 
material was used. 

■pDNA im\.-!niV KEOION SriiVrt:ClKS 

The plastid truL-lrnF region 

incdudes the !r/i\. 



Sampling was definerl on the basis of Cari-ia-Jacas 
et ab (2001), Garcia-Jacas et ab (2002), Susanna et ab 
(2003), and Susanna & Garcia-Jacas (in pr(^ss), in 
order to represent 

most of the genera of tribe 

Introii. the 3' IrnL (UAA) exon. and die inlergenic 
spacer between {rnL (UAA) and iniF (GAA). that were 
ampbried and sequenced [ogcdier. Universal primers 
//vd.-c, forward, and Lni]-(, reverse (Taljerlcl et ab, 
1991), were used lor amplifying the lrn\.-truV region. 
In some eases. /rnU-d. reverse, anil /rnU-e, forwartl, 
were used. Polymerase chain reaction (PCB) was 
conducted in a thermocycler (M.j Research PTC 100). 
The PCK procedure included a warm start at 95'^C for 
1 luinule 35 seconds, followed by 80 C during which 
the pol)ni(Mase (Ecotacp Ucogen S.R.U., Barcelona, 

was added, with 34 cycles of 1 min. de- 
aturation al 93C, 1 min. amiealing at 58 C. 1 min. 

Cardueae. Thu-leen accepted genera {Anipliorirarpos 

Vis., Karvandarina [iecli. b, Iximyropappus Kn(trring -[>^i>f|) 

& Tamamsch.. Lainyropsis (Kharadze) Ditlricdi, Myo- i r i -, ^ • 

, T^ . ,,.; ■ ■ ■ ^17 Ti-- iJi • J ;. extensi()n at 72 C, an( a Inial 10 nun. extcnsum at 

pardon Boiss., Nikunua, OJgueu lljui, Plagiobasis ^.M^ai. i mi ai 

Sclu-enk, Polylaxis Bunge, Russonid C. Winkb, 
Syreiischikovia, Siehcni J. Cay, Tricholcpls DC, and 

72 C. 



PCR products were cleaned with a QlAquick PCR 

Hjin) are sequ^cecl here' b»r the first Purification Kit (Qiagen Inc., Valencia, CA) and 

lin?e. Six other geu<a-a that were not accepted in our sequenced the IruL-c and /r.U-f primers. Dn-eet 

latest revisiouofdielribe (Susanna &Carcia-Jacas, in sequencing of the ampbf.ed DNA segments was 

press) are Aegoponlon Boiss., Anurn, Fmlovia, performed using the BigDye Termmalor Cycde 

Upsrhilziella, Modesiia. and Tmwcarpus, Two more Secinencing v3.1 (PE Biosystcms. Foster City, CA), 

genera, Dolowiara DC. and Himalaidla, were following tlie protocol reconunended by the manufac- 

obtain(Hl from sequences published els<wvhere. Three turer. Nucleotide sequencing was^carried out at the 
onlgroup species were chosen, two among 

Tarcho- Serveis Cientinco-Tecnics of die University 


nantheae and another fnnu the germs OLdenhargia. Barcelona on an ABl PRISM 3700 DNA aualy/ei 

because the trilu^ ami the genus form the sister clade (PE Biosystcms, Foster City, CA). 

to Cardueae (Panero e^ Fiuik. 2002). Man} of our ITSl 

and 1TS2 sequences from previous studies (Garcia- c.,,dna m<(/K (iENE STRATEGIES 

Jacas et ab. 2001, 2002) have been completed with 

the sequence of the 5.8 S gene, and some of our old 


e nave s 


manual bPS se(iucnccs (Susanna et ab, 1995) were re- 
serpienced or connrmed by automatic sequencing. 
Both previously published (Garcia-Jacas et ab, 2002) 
and new sequenecs of the jualY. gene w^ere used in this 
analysis. AU the //7/L-//7;F sequences analyzed are AST-IR (Garcia-Jacas el ab. 2002). The PCR pro- 
new,' with the exception of Dolomiaea (from Liu, cedurc incduded a warm start al 94°C for 1 mm. 

20 sec., followed by SOX dujing Avhich the puly- 

ed the first 1000 base pairs al the 
5' end, l)ecause this part includes most of die 
varialiilily in the malK plastid gene (Hilu & Uinng, 
1997). Partial malK was amplified by PCR with th 
primers /;7/K-710 F (Johnson & Soltis, 1995) anrl 

uu[)ublished) and some si>ecies of Saussurca (from 

Raab-Staube, 2003). The number of new setjuences is merase (Ecotati, Ecogen S.R.b., Barcelona, Spain) was 


Annals of the 

Missouri Botanical Garden 

TiiMc 2. ()ri<i,iii of liie itialciials, hcrlyafia wIkmv the vouchers aiv il('])(>^itr(l, an([ CciiBatik ac.n'ssioii 
se<|iirri{'{'s arr holdlafciij. 


\k'A'S ( 



Ac<ui!liolcj)is oncniiilis Lrss, 
Acrop/ili)!! rcpcfis (L.) IX'. 
Aljmhi! /fcantholcpis Kar. iK Kfr 

AlJh'iHd cernud (I..) (iass. 
Alfrcdia flirca Kai. X l\ii\ 

AmljcilxK! Inramm lljiii 

Ampin incarpos a u I (trial us 
BKhic <Jv iMa\('i 

Amphorifdrpos cxsul (). Scliwar/ 

Arcl'nini lapjm [.. 
Arcliiifn ainiJis l*ciiili. 

AtraclyHs auicclldla \ .. 

AirarfyHs airdiuis (Foissk.) (^Iiiisl. 

Al UK I) lis hunnlis L. 


[IkicI] lodes piponifd I\{)i(l7 
CN Kilani. 

Rcrtu'did sidxtcdidis \ \ 


ItscoltH I ){] 

(icrid (itsciXi)! 

Cfdlicrplmliis nilcns (\1. WuA), 
ex WilM.j C. A. Vl.y. 

Canlopulium coryinhosuni (I..) I' 
(Ainliuici'UiLs dunmxd Hatl. \ I 



Cdrdiaiccllus /ntin'olir'ns (Dclilc) 

Cdvddus carlinoidcs (entail 
CarduNs dcjldrdliis L. 
(^(jrdiiiis pycuovcphdlus I,. 

CdiTind ficrmtliifolid \\\. 

Cdiiind fdleaid S\ cnl. 
Cdrlidd i^uuduifrra (L.) Less. 
Cdflirid IdUdld L. 
Carliiid nidcru[iliyll(i (Dof.) Dt; 

Cdiiidd vida^diis I ,. 



(iarcia-Jacas el al., 2002 
Garcia-.lacas el al.. 2(K)1 
Kazaklislan. Susniuid 
2092 rl dL (lU:) 

(laicia-jacas et al.. 2002 
Kazaklislan. Susaruid 

2090 r( dl. (BC) 
(wircia-.lacas el al.. 2001 

Serbia tK Moiilcncnro, 

Sld'dddiif el (d. 
4.10.<H (lU.) 
Tiirk<'), Susanna 
2256 n dl. (i](: 

Carcia-Jacas cL al.. 2002 
Garciajacus et ak. 2002 
Garci;i-.|acas et al.. 2002 
Garcia-.)a<-as c! a)., 2002 
Garcia-jacas ct ak. 2002 

C^arcia-Jacas et ak. 2002 

Garcia-.kicas ct ak. 2002 


Soiilli \rri<-a. Orliz 20.;^02 


Gareia-Jacas el ak, 2001 

Garcia-Jacas et ak. 2002 
Vikitcrsana ct ak. 2000; 

Garcia-.lacas <■! ak. 2001 
Vllalcrsaiia et ak, 2000 

Garcia-Jacas el ak, 2002 
Spain, (dinialjc 18 (HC) 
Gareia-Jacas el ak, 2002 

Garcia-.lacas el ak. 2002 
(Garcia-jacas et ak. 2002 
Gareia-Jacas el ak, 2002 
Garcia-Jacas el nk. 2002 
Gareia-Jacas r-t ak. 2002 

(iarcia-Jacas et ak, 2002 

Vilatersana et ak. 2(MK1 

Carllidinus crclicus I.. 

Carlhdmus leucnctndos Sihlli. iK Sni. Vihitrrsaiia el ak. 2000 

Cardiannis oxyacdnllid fVI. Bicl 

Cdilhdinus liiiclorius k. 

Vikitcrsana ct ak, 2000; 

(/arcia-Jacas ct ak. 2001 
Vilatersana el ak. 2000 

Cdrfltdddts furkeslanicds Popov 
Cenlaurcd allxt L. 

Cf'nfdun'd (unadancnsis Sch. IJip 

Vilalcrsana el ak. 2000 

Garcia-jaeas ct ;ik. 2000 

Garcia-Jaea^ et ak. 2000 

kkS i 




Aya2622 I 



A Va 2 62 2 6 

















A !■ 140480, 


A ^ 013528 
AYn262 12 
AY»262I 1 



\f:uoi 16 



\FI 10100. 

AFl HMO 1 


AFl JOk^lk 

AFl lOkVJ 
A^ 82 62 19 










VY 7 722 71 





AY7722 76 






AY 7 72 281 

AY 7 72289 




AY7 72293 








\V 78508 







A ^ 013521 
A vol 3522 

AM) 13523 



A vol 3525 


A^ 013 193 

A vol 3527 
A V 785091. 


A vol 3529 

A^ 013.5:52 

A^ 013533 




A^ 785093 


Volume 93, Number 1 

Susanna et al. 
Cardueae (Compositae) 


Tal)le 2. Conllnued. 



Centaiircd belien h. 

Cenlaurea hcnedicta L. 

CenUnirea brugiiierana (DC.) 

Cenlaurea calcilrapa L. 

Cenlaurea carolipauana Feni 

Casas & Susanna 
Cenlaurea cyanus L. 

Garcia-Jacas el al., 2000, 

France, Nan(;y Rot. C/aid. 


Garcia-Jacas et al., 2000, 

Eirvpl, Susanjui 1866 & 

Vilatersana (BC) 
Garcia-Jacas et al., 2001 

Cenlaurea depressa M. Bieb. 
Cenlaurea invohicrata Desf. 

Spain, Garcia-Jacas & 
Susanna 2076 (B(^) 
Garcia-Jacas et al., 2001 
Susanna (^t al., ]995; 

Gan^ia-Jacas cl al., 2001 

Cenlaurea kotschyi. (iioiss. & Heklr.) Garcia-Jacas et al., 2000 


CenUuuea lagascana Graells 
Cenlaurea lingulala Fag. 

Cenlaurea lini folia L. 

Garcia-Jacas et al., 2001 
Carria-Jacas et aF, 2000, 


Garcia-Jacas et aF, 2000 

Cenlaurea macrocephala Muss.- 

Cenlaurea nwnlana F. 
Cenlaurea polyaeanlha \\ illd. 
Cenlaurea rhizaufba C. A. Mey. 

Susanna el aF, 1995 

Susanna ("t aF, 1995 
Susanna et aF, 1995 
Gart'ia-Jacas et aF, 2000 

Cenlaurolhamnus niaxinuis 

Vi^agenitz & Dittricli 
Chardinui orienlalis (F.) 0. Kuntze 
Cheiroloj)hus benoislii (IIumlxMt) 

Garcia-Jacas et aF, 2001 

Garcia-Jacas el al., 2002 
Susanna et aF, 1999 



Susanna et aF, 1999 

Cheirolophus jnaurilanwus 

(Font Quer) Susanna 
Cheirolophus sernpervirens (F.) Poniel Susanna et aF, 1999 

Cheirolophus teydis (C. Smith) 

G. Fopez 
Cirsium arvense (F.) Scop. 
Cirsium echinus (M. Bieb.) 

Cirsium ochrolepidium Juz. 

Susarma el aF, 1995 

Susanna et al., 1995 
Garcia-Jacas el aF, I 

Cirsium palusire (F.) Scop. 
Cousinia alherti Kegel & Schmalli 

Uzl)ekistan, Snsamui 

2048 el al (BC) 
Garcia*Jaeas el aF, 2002 
Susanna et aF, 2003 

Cousinia arachnoidea FiscJi. & C. A. Susanna el aF, 2003 


Cousinia aslracanica (S|)1-(mi<^.) 

Cousinia caespilosa C. Winkl. 

Susanna et aF. 2003 

Susanna el aF, 2003 

Cousinia canescens DC. 

Garcia-Jacas el aF, 2002 

FFS accession 

























A YO 13 508 

A YO 13497 

A YO 13498 






1 ,35878 













A YO 13507 




AY7 72304 

AY 785094 

















A Y3 73670 



A F3 19068, 



Annals of the 

Missouri Botanical Garden 

Table 2. (^onliiuif^d. 


Const nid chrvsdnfltn Kull 

Cousinia cdii^c.sIh lUiii'^t 

Cousima comndlii Fraiuh, 
Cousln'ui (hssccid Km. tS. Kii'. 

Cousinia rsfandidrii [leeJi. f. X 





V « 

ousiuKi i^'nniilijnliu Knit. 
Cou.smiii lidralai i('{i Rege! iK' 



Coiisiiua microciirpd Boiss. 
Coiisuiiii nculxtiUTi lu^eli. f. 
[= Ti.(HV((irpus ncLibducri 

(Roch. r.) 1! 


CoiLsuiia o/iofHudioules Letlel 

Cousijiid ihiIIkIIi uv/is Kiill. 
[=.\niini pallidirirfns (Knil.) 

(A)iisinia j)l{il)lcj)is Sehrenk 

Cousinia polya'pluda RL]|)t\ 
Cousinia pisrpurco C. A. Me). 
Cousinia synlarifnsis Kult. 

Consinia tianslunuca Kull. 

(Afiisiiua In/lora SelinMik 
C^^usinia ninhrosa Riin<2:e 
Cousiniopsis atntriyloides 

(C. W iiikl.) Nevski 
Crocodyliufn i-n'licuin 

(Boiss. & ilehlf.) N. Cafeia 
Crocodjliuin pniniluni (L.) 
N. (^ai(-ia iK Susantia 


Crocodylnini s}ri(iciun Cass. 

Crnjnna crupinastrnm (Moris.) \ is. 

Crnpino ruli:'aris ('ass. 

Cyiuira cornigcni LiruL 

Cynara hnmilis L. 

Dolowiara unp. sp. {0. [ihrlica in 

Kfhinops nircus \\ all. 

ErJniUips pcrsiiiis Sle\. iS. I'^iseli. 
Erhinops rilro L. 

f^chuujps spini)sissiniiss ']\\in 


Eiliinops lschiin^(U}icus B. I-V(|[^.(■ll 
luhinops risrosiis DC. 




Susanna e( al.. 2()0"j 

Susatnia el al.. 2()()3 

Susanna el al.. 2003 
Susatuia el ak, 200.3 

Careia-Jaeas ri ak. 2002 

Susanna <■! ak. 2003 
Susanna el ak, 2003 

Su^anna el iik. 2003 
Susanna el ak. 2003 
Afghan i>lan. DielerJe 

I Hi) (W) 

(/aixaa-jaeas et ak. 2002 

Uzhek i^Ian. Iu>lsi-]\antzv} 

20.6.71 [W: 

Susanna el ak. 2003 

Susantia el al.. 2003 
Susanna et ak. 200.3 
Susanria el ,ik. 2003 

Susanna el ak. 2003 

Susaiuia el ak. 2003 
Susanna el ak. 2003 


Careia-Jaeas ot ak, 2002 

Careia-Jaeas et ak, 2001 jas 

A('^-ia!opliila cretica{] ..) 
Bnis>. .K Mekh-.] 

Careia-Jaeas el ak. 200 i (,is 

Aef![ial<ipln!a pnuulio [\ ..) 

Boiss. .K lleldr.l 

r/arei;i-.|aeas et ak. 2001 |as 
Ccntaiircn crorodyUnn} k.J 

Susannn et ak. i 995 
(/areia-Jaeas el ak. 2001 
Careia-Jaeas (M ak. 2002 
^^rlugak HIanqne 8 (BC) 

Liu (luijiulik) 

Carnalje el ak. 2005 

Cainatje ci :\\.. 2005 
Careia-Jaeas et ak. 2002 

Careia-Jaeas <'l ak, 2002 

Carnalje et ak. 200o 
Careia-Jaens et ak. 2002 










A F3 19069, 


A ¥373732. 








A K3 19070, 

A Y8 2 62 72 


AY8262 71 







A\ 826276 

A F3 1907 1. 












\ > 5386:^ 1 
A ^ 538639 
A F3 1907 k 



A F3 19075, 






AY7723I I 
AY 7723 76 







\Y 7 72:^20 






AY7 72.323 







A ^ 373662 

\^ 01353 


\V3 73679 

A ^ 373677 


A Y3 73676 





AY 785098 

A vol 35.38 
AY 785099 




A YO 13539 


A YO 135 10 

Volume 93, Number 1 

Susanna et al. 
Cardueae (Compositae) 


Tabic 2. Coiilinuecl. 


Frmcniasid halraricd (J. J. Hodr.) 


Gdldditcs lomcntosa Moeneh 
hhp<Hnnlhiin}\ echinopijolium 

(Boiiitn.) Juz. 
Jurinea albicaulis Bunge 
Jiirincd hcrardioide.s (l]uis.s.) 

0. i[(.fT.n. 

Jurinea cdrduiformis Roiss. 

Juridca huniilis (Desf.) DC 
jiuinca Idnipes Rupr. 

jiiruiod niacrocephida DC. 

JnrifU'd rnoilestd Boiss. 2002 

[ =l/ydli)chdete modestii (Bdiss.) 

DiUrieh lK Roch. f.J 
Jurincd moscbus (Hal)!.) R()l)r(>v 

[=JurifU'lla moschus (Ilahl.) 

Juruwd rohusla St^'hn^nk 
Jurincd sp. ineil. 2 [= Modcsha 

ddrwasica (C. Winkl.) 

Kliarad/e & '! aniamseli.] 
Jurinrd sp. inef!. 1 

Jurincd slocchadifolid (Rieh.) DC. 

Jurinea sufjruticosd R.egel 

Karrd/idarina apJiylla 

llccli. r., Aellen &. Esfanil. 
kidscd scrrdluloldes (DC.) 

Creuter & Wagenitz 
Ldmrroj)d})f)Us schdkapUirivus (B. 

Fedtseh.) Knori'. & Tamaniscli. 
Ldniyropsis ryndroides (Lam.) 

Di[lr-i( li 
Lenzca ronijrra {h.) DC. 
Mdn(is<ilcd s(dmdnticd ([..) Britp & 

Myopordan ducheri Boiss. 
Myopardon hyrcanuin (Berinn.) 

\\ a^enilz 
Myopiudan pcrsLcuni Boiss. 
Nikiluua Icptoclada. (Ror-nrn. & 

Sinl.) lljin 
fS'olohdsis syridca (L.) Cass. 
Old('nl)ur<iid intermedia Bond. 

Oli^aed hdldschuaniea (C. W inkl.) 


Gareia-Jaeas et ah. 2(}0l 

Cai'cia-Jaeas et al.. 2002 
Susanna et al.. 200^^ 

Susanna et al., 200.'^ 
Pakistan, Reeliinf^er 2HI50 

{W) [as Ae^opordon 

berardioides Bois^.] 
Careia-.Iaeas el al.. 2002 

Outreya citrduijormis 

Jaub. & SpaeliJ 
Susanna et ab, 1 005 
Susanna et ab, 200-5 


Gareia-Jaeas et ab, 2002 

Gareia-Jaeas et ab. 2002 

Gareia-Jaeas et ab. 2002 

Susanna et ab, 2003 
Tadjikistan, Buhanor 27.0.()1 


Gareia-Jaeas el ab. 2002 

Ukraine. Rama I0:V21 el al. 


Kazakhstan. Susanna 2l()6 

et al (BC) 
Iran, Sojdk 8379 (W) 

(Gareia-Jaeas el ab, 2001 

ITS aeeessidti 










AF3 19081, 

AF3 19080, 

\F3 19083, 


AF3 19082, 






Kyrgvzistan. Poljdkor 29.8.53 AY826296 

Turkey, Susdnna 2267 el aL 


Gareia-Jaeas et ab. 2001 
(_iareia-Jaeas et ab. 2001 


Iran. Carls s.u. (\\) 
Iran, Koelz I62>95 (W) 



Iran, Remdndieri s.n. (\\ ) 
Turkmenistan, Markora 

3.8.54 (LE) 
Gareia-Jaeas (;t ab, 2002 
South Afriea, Ortiz 3. b02 


Tadiikistan. Ka/ue!in el al 




31.5.86 (LE) 





















A YO 1.3509 

A YD T35 II 




A vol 35 11 






Annals of the 

Missouri Botanical Garden 

Tahh' 2. ConliiiiM'd. 



Olgdcd pccfinata lljln 

Olii^odidcla divar'uaid (h'isch. Si 

C. A. Mey.) K. Kocli 

Olii^(*(h(i('l(i ininirna fliolss.) Bri(| 

Kazakiislaii. Susa/uifj 2IH7 

el at. [W.) 
(»ai-ciii-.|a('as el al.. 2001 

(}finj)i)!{lfini l('p!t)l{'pis DC 

Uzlx^kistaii, Tashkcnl l>n| 

Ganl. (HC) 
(;arria-Ja<-as el al., 2002 

Ondpiitflu/n nerrosmn lloiss. 

Ouopordiiin Idurlcmn Willi!. 

Francr, Dijnii Dot. Can!. 


German V, Berlin Hel. (wirtl 

PJiiiiiiis diboresccns (k.) G. L6j)e/ 

G. I. 


Pirnnntdti acdrna {\ ..) Gass. 
Pldjifnhdsis ccnlfniroidcs Sehr<Mik 


Vikilci-h<ina el ak, 2000 |as 
Carlluuniis drhores(('fis\ 
Phi>nus npluieus iFonI (Jiier & Paw) Vilalersana et ak. 2000 |as 

Cdrlltdftms nphaciis] 
Gareia-Ja<-as el ak, 2002 
Kazakk>laii, Susafuia 2LU) 

et al. [MC] 
TailjikislaiK kamcll/i et aJ. 

2:ki.a6 (ki:) 

'l^idjikislan. Hi)ls(hdn(zer 

et al. 27,1.82 (kE) 

Susanna el a].. 199.") |as 
Ccn{dnre<! (h'dlh<i!a\ 

(iareia-Jaeas et ak, 2001 |as 
Centdurcii <^ildiii(n\ 

Gareia-Jaea^ el ak, 2001 

Pol)!dxis iehnuinii iMui<;e 

Po!)lf!.\is ninklcn I Ijin 

Psepliclhis (leall)dfus |\\ ilii^k) 

K. K 


Psenhcllus sj^ilaniciis {Boiiuu.) 


Psephelliis incdnr.scens (DC.) Hols^ 


Psejthclhis pcrsiciis (DC.) Wagenil/ 

CcnIdiiiCd uicdnescens] 

Pscplielliis indcheniniifs (W illij.) 


Psej)licllus xaiilorfphdiiis (!)(k) 

Fiseh. & C. A. Mey. 

Plilifstcmof] djcr (.|ae(].) (^/rfMihr 
Plilo.sfe/noii tlidf'dnfhd (l.ajjilk) 

Ptiloslenntn echinoceplidlus 

(Wilkk) Grcnler 
Ptild.slefin)!! Jiispdnii us (kani.) 



Ixlidpdfitirdules djricdud (Lain.) 

M. V. A-ah. OC Grenler 
Rhdpunlicoide.s hdjdstdna (Tzvek) 

M. Vk '\<i;al). iK (ifeuLer 
Rhdpdnilium acaule DC. 
Rhdpdiificiun dijsfntle 

(("»aink) Snskov 
Russdirifi sngdidna {Wuw^c) 

R. Fe<l|seh. 

Sdussun'd dipiiu! (\ ..) DC. 

Gareia-jaeas el ak, 20(}i |as 
CeiUdured i(dul)ae] 

Gareia-Jaeas el ak, 2001 jas 

Gareia-Jaeas el ak, 2001 [as 

Cc/ildurcd .\(f!}toiej>hdld] 
Gareia-Jaeas el ak. 2002 
Turke>, Susd/uui 2313 el al. 


Ukialne, Ronn) ]()363 el nL 


Spam. Malms S: Cdn\d- 

Careid. kS.9.98 lIlC). 
Susanna el ak, 1 995 

Gareia-Jaeas el ak, 2001 

Susanna r\ ak, !99b 
Australia, Punk s.n. (HC.) 

I'adjikislan, PtolschaiUzer 

5.5.7.") (Ij;) 

Gareia-Jaeas et ak. 2002 

dshulduii (Hjin) ! .i])seli.J 


] rS aceessie 








AF! 10444, 

A Fl 40115 









A^ 012:^19 






\Y«291I I 







Sdussiirea ashukinii lljin [^Prolorid Ta(ljiki>lan. I\<niielin 2k(>.7() AY826:i2 L 




AY7723I 1 
























AY 78,11 09 

AY78r>l 10 


A vol 3549 

AM) 13501 


WO 1 3500 

WO 13491 



VY785I 12 

A vol 3502 


Volume 93, Number 1 

Susanna et al. 
Cardueae (Compositae) 


Tabic 2. Conlinucd. 



Haah-Stranhe. 2003 

Sdtjssurea rdrduicephala (Iljin) lljin Tadjikistan, Srimkoi (K: 

[ = IJj)sclulziella canlukvphula Datpshiafiho 6.8.80 (IT^) 

(lljin) Kaniolin] 

Sdussurca ccrdfocarpa Docnc. 
[ = Lipsi:hilziella ceraloatrpa 

(Decnc.) Kamelln] 

Suiissiirea dvlloidea (OC) Sell. Hip. Raah-Straulx-, 2003 

[ = IIinialaiella dclioldea (DC.) 
Sanssiircd discolor (\\ illd.) I)(^.. 

Cai'cia-Jaeas el al., 2002 

Saiissiircfi rli'i^^ans Lcdeb, Susanna el al., 2003 

SdusMirra frnloivii Lnlcl). [ = FroIorid Raah-Shaulx'. 2003 

froloivii (\.vi\eh.) Raah-Slranbe] 
Sdu.ssitrcd nidxlmoicirzii Herder 


Snsanna el a!.. 2003 

Susatnia et al.. 2003 

Scliisclikuud (dbispino (Hntige) lljin (/areia-Jaeas el al.. 2001 
SvlinidUuiuscnia nidiilans (Re^el) 

Srrrdluld conftiaUi L. 
Siehcnt j)Ud}^c!is (I .am.) DC. 

Silvliuin fiidridnum (I..1 Caertnei' 
Stdchclina Ixuiica DC. 

Gareia-Jacas el al., 2002 
Turkew Sustmiid 2316 c( dl. 


Gareia-Jaeas el al.. 2002 
Gareia-jaeas el al.. 2002 

Sldcliclina duhid L. 

Sldchclina fntiicosd T. 

Slat'lu'lind lidwlu DC. 

Sidi'heliua unijlosculosa Siblli. & 

Slizoloj)lu(s hdlsdjiijtd (Lam.) 

Cass. eN Takht. 
Slizolnphiis cornnojiijtflnis (^ass. 
Synunis p(dnid!opinn<f(iJldus 

(Makino) Kilani. 
Syrcitschilcoiid s})inu!(>sa (Fcaneh.) 

France, (^orrtdfjc 23 (.K: Lidjue 


Greece, Krili, (Uirnaljc 11/ <!^ 

Luqitc (B(^) 
Tui'key, Siisdn/id vt al. 2272 


Greece, Rons t^- Royl 3li9^ 

Berlin Bol. Card. (BC) 
Grareia-.Jacas et al.. 2001 

Gareia-Jacas et al.. 2001 
Gareia-.hicas v\ al.. 2002 



TdrchoiHinlliiis ((iniphiU'dlus L. 

TrlclidlcpLs lihcticd Hook. f. <X" 

Kazaklislan. Susdnita 

22()(} el dl. (BC 
Soull. Alrica. (hliz 17.3.02 


Fakisian, Misscr HISS (15) 



Tugaruwiia iiio/igoltcd lljiti 

Trriinnns leucogniphus (L.) 
Volittdria cntpinoidcs (Desl.) 

Mongolia. TvubiH el al. I . * .89 


Garcia-Jaeas el al., 2002 
Gareia-Jacas el al.. 2001 



Xerdnlhcfnuni annfiiini F.. 

Xeraniheniutn cyUudracvuni Sai. 

J\nkey, Susanna 2362 el al. 


De!iniark, Cojtenhagen B)ol. 
Gar(L (BC) 
Xenuilhcmufn inapertum (L.) Miller Garcia-Jaca.s et al., 2002 
Xcranllicnnun longrpapposiim Kazakhstan. Susanna 21H2 

Fi.sch. tK C. A. Mes. et dl (BC 


IJ'S accession 




A F3 19092, 

AF3 19146 

AJ6062 1 L 





AF3 19095, 

A F3 19149 
























\Y 7 7235 7 




AY 7 72 360 




\Y 7 72 3 64 


AY 7 72 3 66 








AV 7723 77 

AY 7 72 3 79 

AY 7 72 380 






A V3 73681 



A vol 3.551 











A\ 013554 

AY 785 126 

AYO 13555 


Annals of the 

Missouri Botanical Garden 

TahU; 2. Cdiitiniipd. 


ZaegCd halil.schuafiicd C. Wink 

Zoegfd Icpldiirca \ .. 


Uzljt'kislaii, l\li(Ls.\(iiior s.n 


Can-Ia-Jat-as rl al.. 2000 
[as Z. niiiiiiensis 




A YO 12311 




711 a 





added, and 10 cytdes of 45 sec. dciialuralioii at 94"C, 

Tfie ITS 

matrix was analvze( 

:ed by Hayesian in- 

1 min. annealing al S8' C, 2 niin. (extension at 72 C, fercnce, ])reaurie heuristic par^iniony search was 
and a linal 10 min. exlensiun at 72"C. W'A\ pnxhu'ts impossihle due lo die si/e of the (hita tnalrix (1 00 
were cleaned with OlAt^nick PCK Purification Kit species; the search for mosl-parsinuHiions trees was 
(Qiagen Inc., Vahaicia, CA) and se(|uenc'ed with IniK- too llme-cunsumina; and soon became nnpraetieal). 

Hayesian inference (HI) esliniation ^vas ealcuhited 
atupiified DNA segments was performed as h)r the using MrHayes ;5.() I (Roncjuisl & 1 luelsenHcek, 2003). 

I he hest-a\allal)le model of moleculai- evoiulion. 

re([uired for Hay(^sian estimations of |>hylogeny, was 

liierarclneal likelihood ratio tests 

i iO y and AST- I I! primers. Direct sequencing of th<^ 

fniL-lniF region. 


s(decled using 

(hidi r) and Akaike inlormation criteria ( AlC) as 
The three nuclear [TSl sfiaeer, 5.8 S gene, and Implemented in the software MrModcltesl l.ll. 

I rS2 spaeer (the ITS region) were amplified and (Nylander, 2002). which considers only nncl(M)lide 

seqn(Mieed logellier. Th<- ITS region was amplin^MJ hy sid)stitution models dial are currently implemented in 

veil with 1406 K (Nickrent et ah. lOOd) and ITSl PALP and MrBa>es 3.01 (IhieLsenl)eck .H Hon(inisl, 

(White et al., 1090) as forward primers, and ITS I 2001; KoiKimst & Hnelsenheck, 2003). The I)esl-fil 

(\\1nte et ah, 1990) as reverse^ primer, referring to the model of nu.deotide substitution for the ITS dataset 

l)ro[ocol described \n Sollis and Ku/off (1993). P(d{ was the same in both m(^lhods: the s\anm<4rical m()d(d. 



w ere 




using the QIAqnick PCM 

with some sites assumed to be hnariabU" and \ariable 
sites assutned to follow a discrete gamma dlstribnt ittn 

Purification Kit (Qiagcn Inc., Valencia. CA). Se~ 

(|uenclng ])rlniers 1406 F and ITS4 were used. Direct (CTR + I-Hf;; \ang, 1996). Hay.\sian inferfMice analyses 

sequencing of the amplified 
[)erloiined as for the lni\.-fniF region. 

DIN A segments was 

were initialed with random starting trees and were rim 
for 1 X KV' generations. I'our Melropolis-coupled 

MarkoN chain Monte Carl 




puyi-oci'Nm'n: an\i,vsis 

ns wcj'e 


sampled every TOO generations, which resulted i 

10,000 sam[)le trees. A critical aspect of the Ha\esiau 

Nucleotide se(|uenees were edhcd with Chromas analysis is to ensure diat the Markov chain has 

1.56 (Teelmelyslmn, Tewantln, Australia). The //7d.~ reached stallonarity. All sample points prior to 

IniF and malK s(MpHMices were aligned visually by stationarit> are <^ssentiallv random and are discarded 

sequ<aitial iiairwise eomparison (Swofford 6^ Olsen 

as 'Inu-n-in" 1,000 >amples trees, because they do not 

1990). The fUdlK sequences were translated for their contatn ns(^fnl parameUM" estimates. Intcrnodes with 

putative proteins willi Genejockey (Hiosoft, Cam- po.-,terior |>robabllllies > 95% were considered 
bridge, U.K.) to verif\ the al)senci' of inLernal stop 

eod(»ns among those for amino acid codons. Due to die tn^e was calculatcnl with PALjP version 1.(}|>l.a (Swol- 

high level of variability of the ITS se(iuences, our h.rd, 1999). Postimor probabdily supjiorl (PP) was 

statistically significant. A majority-rule consensus 

allgmnent was checked with the ITS alignment h)r the 
wliole Composita(^ by Coert/cn et al. (2003) and 

esliiualed t(t be slgudu-ant for nod(^s w 

ith PP 


Foi" the c(»mbined data sets, parsimony anaUsIs 
adjusted manually. In order to conserve the phyloge- involved heuristic searches conducted with PAPP 
ucLIc information of insertions and deletions that 

v(M'sion 4.01)10 (S^vofford, 1999) using Tree Hisection 

constituted most of the variation of the tniL-lniF Recognition (THH) branch swapping widi character 
region, and at the same time iwiml an overestimation states specified as unordered and unwcigliled. All 
o( lengthy indels, they were coded as presence 
absence characters and addetl to the end of matrices 
in the combined analyses. The afigned data nuilrices 

most j)arsunonious trec^s (MPT) wei'e saved. To locate 
islands of most parsimonious trees (Maddlson. 1991). 
■s we performed 100 replicates with random taxon 
are availal)le on request from the corresponding adihtiou. and with THH branch swap[)ing. Tree 
'^i-'lhor. lengths, eonsisteiu'y index {CA}, atid retention ind(^x 

Volume 93, Number 1 

Susanna et al. 
Cardueae (Compositae) 


Tal)l(' 'A. {'omparison of rrsuils from llic ITS, ITS + IrnL-lrnF, ant! ITS + IrnL-lrnV + mntK data sets. TIk^ consislcncy arul 
homoplaRV iiKlicrs an^ (-alciilated \)\ exc-liidin^ uitii]tontiati\'o characters. 

Da la set 

IN 1 1 ml 

m nor o 

r ta\i 

Total charaotoi-s 
lnformali\ o cliaractiM's 

NunilKM- of MITs 

Numljcr of slojjs 


Conslstoncy Ind<'\ (CI) 

Retention index (RT) 

Homoplasy index (1 II) 

Range of di\ crtience. ingronp (%) 


1 90 






ITS + iniL-lmV 


1 r>99 








ITS + lrn\.-!mF + watK 








(RI) are always given, excluding 

uiiinfoniiati\ t 

consensus trees of ihe t^vo condiined data sets are 

charaelers. Two eomhined analyses were performed. larii^dy coincident willi ihe parsimony consensus trees, 
with dirferenl data sets: tlic ITS + /rnL-/rnF sequence and iherefore we have added llie Bayesian support 
data and the ITS + lrn].-frnF + matK data. 

(PP) to ihose branches that liave PP > 0.95 liul are 

Bootstrap (BS) and Bremer support (Brcnier, 1988; not, or arf 

^ oni\ 

]y weakly, supported by parsimony 

Donoghiie et al., PJ)92) or decay index (DI) were 

carried out to obtain support estimates for the nodes in 
the consensus trees. Bootstrap analysis was [jerfortned 
(Felsenstein, 1985) using 1000 replicates and heuris- 
tic search with Uie default options. Tti the urDNA llS 
data matrix, we used llie a[)proach by Liden et al. OElJMvA rioN OF camdckak 

(Pigs, 2, 3). Only the Carlininae branch in the 
cond)ined Bayesian analysis of (he thice regions is 
illiistraled (Fig. 4), because it confirms the position of 
Tuixar'uioi'la within Carlininae. 

(1997) using 1000 replicates, random ta\on afhhtion 
W4th 20 replicates, and no branch swapping. lM)r the 
two combined matrices, DI was calculated for each 

le 1 

n(Kie oy successive analyses using 



le c 


e con- 

straint approach, as discussed in Morgan (P)97), with 
10 rephcates. ACCrfRAN (acce]erate<l Iransformation) 
character-state optimizalion was used for all illustrat- 


1 tr 

Ri:sL las and OiscrssioN 

Ihe monophyly of Cardueae was confirmed uith the 
new outgrotip in all the analyses wnTh high statistical 


t: PP 

1.00 (Fig. lA), BS 

1009(^, 100% 

(Figs. 2, 3), and 1)1= II (Figs. 2. 3). Thus, the most 
api>ropriatc status for Echinopinac and Carlininae is 
subtribal. fndeed. Cardueae could be divided into five 
trilx^s, but we consider it unpraclical to fraguKMit 
a natural grou]) that can be so easily recognized on tlie 
basis of macromorpliology. 


Since we were miablc to obtain DNA se(|uences for 
all three genie regions for eveiy taxon sampled, we .p,^^^ j-^,,,. ,,j},,,i],^^ recognized by tlie lat.'st report 

pcrform.'d three distinct analyses: (1) ITS alotie, to ^^^^ j,^^ ^^.j,.. (Carcia-Jacas et al., 2002), Carlininae, 

examine the j)osilion oi some genera n(^ 

f .^ 

t included in 

Echinopinac, Cardulnae, and Centaurcinae, were 
previous analyses and for which we w^ere not able to confirmed. Subtribe Cardopatiinae must be restored 
amjjlify any chloroplast region; (2) ITS and frnl.-lrnF 

regions combined, to stud} the generic Inmts ni 



and some changes made to 



m o 


plulogeny and subtribal didineation. Ilow'ever, in 
Saussurca group; and (3) the three regions (ITS, IrnL- ^,j^.^^ ^^f^]^^ moderate support for these basal branches 

//7/F, and f!}(}{K) combined, to elucidate subtribal 
limits and to confirm the naturalness of lh(^ informal 

(the) ciihapse in a ])olytomy in all the Bayesian 
analyses, i-f. Fig. lA), subtribes (Carlininae. F(4iino- 


groups in Carduinae. The numeric results of the three pinae, and Cardopatiinae should be considered 

analyses are summarized in Table 3. The resuhing ^ euirently unresolved polytomy basal lo Carduinae 

trees are shown in Figure lA and IB (Bayesian 

majority rule consensus for the ITS dataset alone). 

Figure 2 (parsimony stricd consensus of tiie combined 

ITS and IrnF-lniF sequences), and Figure 3 (j)arsi- 

mony strict consensus of the combined ITS, //7^E-/rnF 


Our results do not morlify the cinannscription of 
and ma/K se(juences). The Bayesian majority rule Carlininae in our latest surveys of Cardueae (Garcia- 


Annals of the 

Missouri Botanical Garden 












^ _ 































CJrsium iKhrofcpiilnim 

C irsium arvense 

Cirsium echimts 

Cirsiam palustre 

( urduiis Viirlinnhlvs 

i iu'iiuus ik'floratiis 

Cartluus pyaiocL'p/iufiis 


SUyhufu puirhutuni 

I^olohusis syriaca 

P'uiiOfnon aciinm 

Cyttani cornij'cru 

Cynura hum/Iis 

Ciilia tiles tonicntosii 

I.amyropsis iynaroUlcs 

Plilostcniati afer 

PtUt^stcmon uhianitha 

Pti(f>stcm<>n hisnanuus 

Pliiosttnuiii cchiiiiHcphiilus 

Juriuea bcrunfiohies / Acyoponli^nJ 

Jurincu cuniuiformis f OufrcyaJ 

Juriuea hinipcs 

JurifU'ci robustii 

Ji/rinru suffrutlcosa 

Jur'meu sp. 2 j -MtHlcsthij 

Jur'nicu matTOL'cphala 

Jurinca ulhiiuatis « 

Jiirniea sjk I OBUSSUrea 

Jurinea nuniUis n fO U D 

Jurincu stijcchailififfiu " ^ 

Jurhwii moM'hiis / JurincHaJ 
Jurincu moilestu j IlvaliKhaclcl 
Saussurea curJutcip/iala / LipschiizicUaj 
SausMtrea ceratocarpa j- l,ipschi!::icUa] 
Situssnrcii ilcluudai I irunaUnclUjI 

I rt»l(fviis/ 



Dolouiiiwa tibciica 
Siiiiwureu ushukinii 
SausMireu frohnvii 
Palyfifxis Ivhmunii 
Polydtxis wiiiklvri 
Sauwurea afpina 
Siiiiss urea tiiscolor 
Saussurea cU'^'uns 

Suuwureu fnuAimtm iLzii 
Cousiniu paUiiihirens j 
Cousiuiti luppmea 
Cousiuiu uiherti 
Cou\iuia rri/iora 
C (fusinia karatavica 
C()!i\inia umhrosa 
\nfiuuf luppu 
Arctium uiinus 
Cousiniu ''rantli/t^/ia 
Hymuauihiuni evhinonifoliuni 
Schmulhau\enia niiluhins 
Ctuisinia dissecra 
Cousinia chrysuuthu 
Cousinia p(ffycvp!iulu 
Cousiniu synlaricnsis 
( ousinia Uausluiniea 
Cousiniu eaespitosu 
Cousinia ctui^esfa 
Cousiuiu pliiiylepis 
Cousinia urulitnoidca 
( ousiuiu astracuniia 
Cousiniu euncscc/ts 
Cou\iniu onopordiiiides 
Cousinia purpurea 
Cou\iuia esfundiarii 
Cousiuiu neubaueri [ --Tiarocurpasj 
Coifsiuia coronatu 
Cousinia miennurpif_ 
Alfrediu ueuntboiepfs 
Aljrediu nivea 
Alfrediu cernua 


l.umyropappus sehukupUirtcus 
Ol^idea biildschuuuii a 
Oti^aca pevtiuala 
Syuurus pu!maft}pinnulijidus 
Syreitsehikoviu spinu/osu 
Onopordum leptolepis 
Onopordum nervosum 
Oni}pordum tauriium 

Berurdia > ui}acuulis 
Stuehelifia huetiea 
Sme/relina dubia 
Suiehelina uniflitsculosa 
Staehelinu fnitieosa 
Suwhelina loijelii 
A nipboricurpos aufuriatus 
Afupbifricurpus e.xsul 
Chardiuia orietUalis 

Sivberu puni;ens 
Xerauthemun} anunum 
Xeranthemum iuapertum 
Xetunlhemufn loff}^epapposum 
Xerunthemnm cylinanueu/n 
Airuetyiis cancelfufu 
Atrucfylis earduus 
Atraeiylis humifis 
Curlinu ucunlbi/o/iu 
Carlina falvutu 
Carfifut lanafa 
Carlinu vub^aris 
Carlina liumntifcrn 

Carlinu nmcrophylla 
A t rue fy lodes j upon it a 
Tu^'urinoviu o uniiudjeu 
Curdopatium corynihosuui 
Cousiniopsis afrue/yfoide\ 
bruibylaena dtseolor 

Tarchonanthus eumphorufus 
O/deuhur^ia intermediu 







!■ t<iiiit' I . (pji. 1 (yl-\W.\). 

A (p. 162). Haycsian inajorily rtilr consensu^ tree ofllir ITS .sc(]iiciic( tlala malrix (hasal pari 
of the Iree only). Numhcrs iihovr hrari('lir> are Haypsian Poslcri-n" I*iohal)ilili('s (PP). (■AKI)()P,'\1^ = ('anlopaliitiac - 
16,"^). na)f.sian iiiajorllv rule coii.seiisus tire of llie ITS .srqu(Mic<' dala irialrix (ii()pcr pari of ihc trcr (ttilv). Niiinlu-rs above 

H (p. 

hraiuTcs an- Ha)('siaii Po.slrrior I^ohahililirs iW). 

Volume 93, Number 1 

Susanna et al. 
Cardueae (Compositae) 






























Acaittfiolepts onentalis 

f'c/ii/iops niveiis 

fi:"ui;:':^[r' , echinopinae 

hcli'uiops fschhn^ii/iicus 
Ecliiftops spinosissimus 
Ec hi turn s viscosus 

AiT<tpni<in repcns 
Leuzea coitifera 
Myoponhn auchcri 
yjyopordon hynanum 
Oligochucta divanciUu 

Oli^ochacta nihilmti 
Myoporihm persicutfi 

Rhiiponticum acaiite 
Rhiiponncum iiustnilc 
Crocodyfiiim crcticiim 
Crocodylium pumilum 
CrocoJyIium syr'nunm 
CardimccKus duvuiixii 
Curdunccilus mureolicus 
Femenius hi balciinca 
Phonus arboresiens 
Phoniis riphueiis 
Carthamus cretkiis 
Carthamus }eua>caulos 

Curthiimus furhcsluniciis 
Carlhamus oxyacantha 
Carlhamus tmctorius 
Centem/ea u/intdtitwusis 
Centaurea kolscUy} 
Centaurca rhizantha 
Cciilanreit nuicroccphafa 
Ccfiliiurea bchen 
Centaurea hru^Jiuicruna 
Cetilaurea cala'rnipa 
Ci'tUaurea nnolmnila 
Centaurea polyucufif/ia 
Centaurea linifoiia 

Centaurea benedicta 
(enlaurea cycinus 
Centaurea depressa 
Centaurea lin»ulata 
Centaurea montuua 
C enfaurea earolipauana 
Centaurea lagaseana 
PsephcHus pukherrinms 

Psep/ie/Ius dealbatus 
PsepheHus }^ilunicus 
PsephclUis pcrsicus 
Psephelius iucaneseens 
Psepbellus xanthiicephulus 
Amberboa turanica 
RussoH'ia so^^diana 
Plauiabusis eetitanruides 
Caukepfialus nitens 
Karvandarinu aph ylla 
Rbaprtntieoides afrUana 
Rbaponticoides hajastana 
Centaurnthaninus nuLximus 
Cbeirohpbus bcnoistii 
Ch eirnioph us ma uriian ic us 
Cheiroloph us sempervhens 

L Iteindoplius teyais 

Crupina crupinuslruni 

Criipina vulgaris 
Mantisaha salniantica 
Serratula vortmata 
Sikh'inh} leptocfada 
Klasea serratuloides 
Trieholepis tiheticu 
Volutana erupinoUles 
Zoe^iea leptaurea 
Zoe'f^ea buldshuauka 
Stizoloph us halsamita 

Slizoloph us coronopiJoUus 

Sebiscltkinki afbi's/fina 


Mgurr 1. Continued 

Jaf'cis c\ al., 2002; Sii.^aniia & Garcia-Jaras, in press). genera thai were classified by oilier authors (Diltrich, 

The sul)lnh(^ is monophylcUe without Bayesian 1977, 1996b; Bremer, 1994) in Carliniuae belong 

support in the ITS analysis (PP ^ 0.89, Fig. lA) either to Carduinac (5/arAe///(r/ anil the Je/a////K'//;z/m 

and with high support in the combined analyses (BS ^ gi'onp) or Cardopaliinae {Cardojxiliun} and Coushdop- 

95%, Dl -^ 7. Fig. 2; BS ^ 100%, DI ^ 9, Fig. 3), sis), based on niohxular phylogenics as suggested by 

and includes Alraclylodes DC, Atmrfylis, Cadina L., the secjuence data. The classic definition ofC^ailininae 

and Thcvenoiia DC. (not !U(du<led in j)resent analyses, was based mainly on achcnt^ charact(Ms (Diltrich, 

but confirmed in oiu' previous work). The remaining 1977, 1996b): parenchymatic pericarp usually hir- 


Annals of the 

Missouri Botanical Garden 

























100 13 



Saussurea group -/I 




















Arctium ^Toup 1 



















80 2 

Saussurea group 








Carduus group 




















Onopordum group 






Berardia and Staehelina 







Xeranthemum group 





























Acantholepis orientalis 
Echinops niveus 
Echinops persicus 
chinops i^chimganicus 



c hi nor) 

s viscosas 

Tuqannovia monqolica 

Acroptiion repens 

uzea conifera 


aponticum acaule 


Oligochaeta aivaricata 
Oligochaeta minima 
'^haponticum australe 

emaurothamnus, maximus 

dyUum crettcum 
rocodylium syriacum 


Carduncellus duvauxii 


F&meniasia balearica 
'"bonus rip. 
arthamus creticus 

us riohaeus 

arthamus turkestanicus 
arthamus oxyacantha 
entaurea benen 

Centaurea bruguierana 
'^entaurea involucrata 

entaurea carofipauana 
Centaurea lagascana 
Centaurea depressa 

Centaurea lingulata 
Psephellus pufchernmus 
Psepheilus persicus 
PsepheUus gilanicus 
Calficephalus nitens 

heiroiophus mauritanicus 

heirolophus teydis 
Rhaponticoide$ haiastana 
Crupina vulgaris 

Serratula coronata 

'Ja,sea serratufoides 
'olutana crupinoides 
gegea leptaurea 
tfzolophus balsamit^ 
tizQiophus coronopifoiius 
chiscnktnia albispma 




Junnea berardtoides [=Aegopordon\ 

Jurinea carduiformfs [^Oinfeya] 

Junnea rqbusta 
unnea atbicaulis 

aussurea carduicephala [-Lipschitziejla] 
aussurea ceratocarpa l=upscnitziella\ 

Saussurea de{toidea[-l-umaiaielfa\ 

""olomiaea tibetica 
aussurea asbukipii l-Frolovia] 

frolovii \-rf(vnvta'^ 

urea rro 

rciium lappa 

rctmm nitnus^.^ ,. AmUr^iH 

ousinia grandifolia MrciiOia 

Hypacantnium echinopifolium 
Schmalhausenia niduians group 

ousinia lapoacea 

ousinia tnfiora 

ousinia umbrosa 

ousipia astracanica 
ousmia purpurea 

ousinia pofvcephala 

ousi,ni,a purpurea 

ousipia neubaueri [= Tiarocarpus 


ousinia cofonata 
sinia microcarpa 

Polytaxis lehmanii 
aussurea efeg$n$ 

aussurea maximowiczit 
irsium ochrolcpidium 
arduus carjjnoides 
arpuus aefloratus 
nrpnus leijcographus 
Irsium echinus 
irsium palu^tre 
ilybum pianapum 
Otobasis synaca 
icnomon acarna 
Galactites tomentosa 
Ptilostemon afer 
PtHostemon diacantha 

i^amyropsis Qynaroides 

nara c 

CVnara bumitls 

Cynara cornigera 

Alf/edia cQrnua 

Alfredia nivea 

Lamyropappus schakaptaricus 

Oiqaea baiaschuanica 

Ofgaea pectinata 

Synurus palmatopinnatifidus 

Syreitschikovia spinulosa 

nopordum nervosum 
Popordum tauric\im 

erardia sutyacpulis 

taehefina du^ja 

taehelina uniflosculosa 
taeheiina fruttcQsa 
taeheiioa lobeiii 
mphoncarpos autariatus 
mphortcarpos exsui 

hardinia onentahs 
ebera pungens 
eranthemum annuum 
eranthemum inapertum 
eranthemum lonaep apposum 





CardQpatium corymoosum 
Cousmiopsis atractyfoiaes 

Atractvlis cancellata 



tracfyhs carduus 
arltna acanthifofi 

arlina falcata 
arlina lanata 
arlina gummlfera 
arlina vulgaris 
tractvlodes laponica 


Brachylaena discolor 
Tarchonanthus camphoratus 
Oldenburgia intermedia 

Im^ur' 2. Slrid ronsrnsiis tiee lA' \Uc most parsiitionimis trees n^siilliiig (roiii lUr FI'S and !rn\.-!rnF cnrnhtiH'd <lata nialrlx. 
RoKlc'd luirnln'i-s are RaNcsiaii Posterior Prol)al)ilities (PP) wliieli are detailed i>ni\ fer l)raiielies iinsi][)fK)rt<-d l)\ parsitnoiu' 
l)oots(ra[). ^UI^l^ers ahove hranelu-s or IxTore a slash are l)ootslraf) [)erceiila<ie> (15S); Ih;Iovv hraiiehes or afti-r a slash, decay 
in<!iees (1)1). A dash itidieate^ honlstrap .sup|)ort h'ss than .'){)%. Ahljieviati(Mis of siditnhes: CP = Carliiiiiiae; CP = 
Canlopat iinae: VX.W = l-'eliinopinae. 

Volume 93, Number 1 

Susanna et al. 
Cardueae (Compositae) 


Acantholepis orientalis 
Echinops nivQus 
Echinops persicus 
Echinops tschimganicus 
Echinops viscosus 


A en 

cropUlon repens 
Rhaponticum australe 
Leuzea conifera 
Rhaponticum acaufe 
Oligochaeta divaricata 
Olfgochaeta minima 
Canicephalus nitens 

Bentaurothamnus maxifnus 
neirolophus mauniamcus 
Cheirolophus teydis 
Serratufa coronata 
Klasea serratuloides 
Volutaria crupinoides 
Crocodylium creticum 
Crocodylium syriacum 
PsepheVus pufcherrimus 
Psephellus persicus 
PsepheHus gilanicus 
Carduncelius duvauxii 
Femeniasia balearica 
Phonus riphaeus 

Carthamus creticus 
Carthamus turkestanicus 
Carthamus oxyacantha 
Centaurea afba 
Centaurea behen 
Centaurea bruguierana 
Centaurea involucrata 
Centaurea carolipauana 
Centaurea lagascana 
Centaurea depressa 
Centaurea lingulata 
Bieizia hajastana 
Crupina vulqaris 
Zoegea lepfaurea 
~tizofophus balsamit^ 
tizQfophus coronopifolius 

_ 'zr.hkinia albisoina 

Arctium lappa 

Arctium minus 

Cousinia grandifolia 

Schmaihausenia nidulans 

Cousinia lappacea 

Cousinia tnflora Arctium 

Cousinia umbrosa Mrcuuiii 
Cousinia astracanica grOUp 

Cousinia purpurea 
Cousinia polycephala 
Cousinia neubaueri [=Tiarocarpus 
Cousinia coronata 



. unnea a 
Jurinea robusta 

J urine a carduiformis 

Saussurea elegans 
Saussurea maximowiczii 
Cirsium ochrolepidium 
Carduus carfinoides 
Carduus dehoratus 
Tyrimnus feucographus 
Cirsium echinus 
Cirsium palustre 
SHybum marianum 
Notobasts synaca 
Picnomon acarna 
Galactites tomentosa 

PtHostemon afer 
PtHostemon diacantha 
Lamyropsis cynaroides 

Cynara cornigera 

Cynara humifis 

Aifredia cernua 

Alfredia nivea 

Lamyropappus schakaptartcus 

Olgaea baidschuanica 

Ofgaea pectinata 

Synurus pafmatopinnatifidus 

Syreitschikovia spinulosa 
Cfnopordum nervosum 
Onopordum tauricum 
Berardia subacaufis 
Staehelina dubia 
Staehelina uniflosculosa 
Staehelina fruticosa 
Staehelina lobefii 
Amphoricarpos autariatus 
Amphoricarpos exsul 
Chardinia orientalis 
Siebera pungens 
Xeranthemum annuum 
Xeranthemum inapertum 

_ ardopaiium corymbosum 
Cousiniopsis atractvloides 

Atractyiis canceHata 

Atracfylis carduus 
Carlina acanthifolia 

Carfina fafcata 

Carlina lanata 

Carlina vulgaris 

Carlina gummifera 

Atractvfodes iaoonica 


Brachylaena discolor 
Tarchonanthus camphoratus 

Oldenburgia intermedia 










Figurr 3. Slricl consensiLs Ircc of llu- most pursiiiiuni.ius lives resulting frnrn llie ITS. ImL-lrnF. and nuitK comhine.l .lata 
maliix. Bokled nuinliers are Bayesian I'oslerior I'rolialiililies (PP) ,letaile<l ouIn for branches unsuiiporte.l \>y piu^lnuniy 
l)ootslra[). Nuniliers ahove l)ranehes or hefore a slash are hoolslrap pereenlages (BS); l)eh>w branches or after a shish, dcriiy 
imhces (DI). A dash in(hcales llo„l^,tra^ supporl k-ss than 30%. Al)breviali(>ns of snl.lribes: CL = CaHininae; CP - 

Cardopatiinac: ECH = EcliiiiopituM'. 


Annals of the 

Missouri Botanical Garden 





1.00 ^ 





A tract}?! is can eel lata 

Atraciylis cardans 
Carlina acanthifolia 
Carlina falcata 
Carlina lanata 
Carlina vulgaris 
Carlina gummifera 
Atractylodes japonica 
Tugarin o via mongolica 

r^I^urr 1. 

Detail ol iIk' hiaiii-li of the suhtribc Carliiiinae fnHii tin- Ba\esiaii tiiajnrily rule cons^-nsiis oftlii' ITS, //7j|.-//7iF, 
am! mat\\ comhiiHM] <lala nialri\. Nmnhcis above liraiu-Iirs arc l]a\csiaii I'o^U-rior I'lohalnlilles (TM'). 

siUi:, and papinis sclae verv 1 

(I i recti} allachfd to the pericarp. However, ll 

oiig AVith ])luniose 


EcluiK)j)iiiae. It is teinj)[!ii<i to ifiter|)r(4 llic c()r\ nihose 
inflorescence of Cardopatiunu foriiKMl hy v(M'y small. 



charac-tcrs ^ niusl he inlcrprelcl as plesion.orplnc. fe^^-^hn^(u•e(l capilula. as a lu-st step towanls swiceph- 

aly. On (his basis. Petit (1997) considcrctl Cardopa- 
Inun sist(^r to Erhinops L. and [)Iac(Hl Cardojuitinm 
and C()!isinl()j)sis in Kcliinoplnac. On the hasis of oui' 
results, we prefi^r to inlerprel these sinu'larilies as 

hecanse tliey appear across all hasal 
((^arh'innac, Cardopaliiuae. and EchinopiiuK;) and 


oniv on acMene 

even in Carihiinae. If we relv 

characters for classification, the jx^sultin-r definition 

s itfcatlv 

of Carlininac (Diltrlcli. 1977, I996h) diffcn 

from the delineation on the hasis of DXA sc(iucnce 

anal)ses and ]nai'ronu)rpholo<;y (Susanna & C/aicia- 
Jaeas, in press). 

Our molecular anal)ses confirm lliat Tugarinaiid. 
a |)ii//llni^ monolypic genus oC (lioccious ]}hnits from 
Mongolia that was placed in Carliniuae h\ Dittricli et l-:(.iiiM)i'i\ \K 

convergence, l)ecans(- synccjjiialies at various states 
of d(weIopmen| in\(>l\ina' sma 




occur in all the suhlrihes across Cardneae (Carcia- 
Jacas el ah. 2002). 

tciongs to Oardtieae. Curionsix . 



w iKivesjan 

1 .0, 

ah (19;!7). ludo 

snhtrihal phicemcnt is supported only h) 

comhincd anal) sis of the []\iva: regions (PP 

Fig. 4). Indeed, lh(^ onlv suhlrihe whcr(^ it can he 

[)laced on the hasis of morphological affinities (leaves, 

in\ohicial hracts. and [tappus) is Carlininac (I)itlricli 

el ah. 1987: Susanna .K Carcia Jacas, In press). Our '^^**l*'*'^'l-"- ^^'^'^ Iiulicalcs that Acandudqns is a rc- 

analyses sliou no ctmnection of Tu^rarinoria with the *'"*'"''" ^"'^^'"'''*''' species of luhlnops (Carnatje et ah, 

only other Kasl Asian representative of CarHmnae, 2()()o). as originally (lescrihctl (/':c/u'/;o/;a (/a/////n.^^^^^ 

Atraclylodcs, or widi anv other -eniis of d.p mihi.ilu^ J^'^^'*" ^^ Sj)ach). Our comhim'<l analyses reveal thai 

Our results demonstrate, conlrary to our previous 
studies (Garcia-Jacas cL ah. 2002). tlial Kchinoi)iriae 
nielnde only luhiiiops s.h (lu-hinops aiid Aauilholrpis 
hess.) uith strong support (PP = l.(){). hig. 1 R: BS - 

= 26. 30. Figs. 2. 3). In hicl, a rectMit 

100%. 1)1 

re i n f^ 

orcnig Its isolatc(J [losilutn. 


* * 

the Xeniiithcmiuu gi'oup does not belong to Fchiiio- 
pinae, hut rather to f^arduinae as sisler to the rest of 

C\IU)0]>,\Tit\ \l-: 

this suhtrihe (Figs. lA, 2, 3). 


t F 

le origui of tile com])ound inflort'sccnce 



This suhtrihe had moderate suppiirt in 
parsimony analyses (BS = 63%, ol%; 1)1 ^ 

4. 6; 


Echij}()j)s cainiot he irackcvl oti molecular 
Ix'caust' llu' suhlrihe does nut show su]iported affinily 
to any other grouj) in Cardueae. Cardopatiinae and 

Figs. 2. '^). perhaps ihie to the diffcnait (wolulionai-y 

rates of annual Cousitiiopsis and peremiial Cardopa- Carlininac are the hesi candidates for sisler groups lo 

I'uuii. The Rayesian support for lliis hraiich, however, the suhtrihe Fc^hifuipinae (hecanse tli(^ structure of the 

is very high (PP - ].()(), Figs. hV, 3, 4). 

Suhtrihe Cardttpaliinae, as first denned, included 
only llie east Meihlcrrancan genus Curdopalnuu. 
Later, fMe\ski (1937j descrihed a mouoty])ic genus 
from central Asia. Coiisi/nopsis, closely related to 

achi-nes is very similar, ch Dittricli, 19/0. 

CAKDi t\Ai-: 

mouoph)-lctie Cculaiuxanae are i-ecoani/ed as 

Cardopahmti (it was (irst descrihed as Cdrdopalinm a distinct suhlrihe. the Carduinae couslilute a para- 

alnulyloides C. \\ inkier). Classic 
Com|)osllae (Benlham. 1(573; I htfhn; 

monographers o 

f phxicllc assemblage (Figs. h\, 2, 3). II 

o\\('\ er. 

uni, 1P>94; Dit- allcrnate solutions aic not practical. Fitlu^r a suhtrihe 

trich, 19//; Bremer, 1991) consistently |)laccd both level is ascrilK^I 

genera among Carliniuae, but the onlv characters lliat 

to all ihe monoplu letic groups 

recogni/ed in present ('arduiuae and a fragmenled 

cormecl these two groups are lliose of achcnes. which classificatl 

could e(|ually relate Cardopuliinu and Cousiniopsis to Carduinae, including Cenlaurcinac, is iiiaiutained. 

on results, or a single large suhlrihe 

Volume 93, Number 1 

Susanna et al. 
Cardueae (Compositae) 


which thereby en(H)rnpasses ahiiost ninety per cent of that tlie inflorescence of Xeranthemum uas not 

the species of tlie Irihe ((iarcia-Jacas et ah, 2002). 

a syneei)ha]y. Indeed, th(^ Xemiuhcmum group 


\en \u 

tills disparate assemhkige, some well- appears, in the (M)nihined analyses, as ])arl of tlie 

defined groups emerge, together widi giMiera uilhout 
known affinities like Bcrardia or Slaehelina. 

iiKR\f<nf\ AM) sr\i<ni<iJ:\A 

Carduinae, sisler to the rest of the suhlri])e, with low 
parsimony bootstiap suppoil hut xciy high Hayesian 
suppoi-t (hP = im Figs. lA, 2, 3), in an isolated 
position, riie monophyly of ihe grou|) also has veiy 

high supi^ort (PP- 1.00, Fig. lA; BS = 100%, DI = 

Our molecular analyses show that these two genera 23, 28, Figs. 2, 3). Traditional classification (Diltrich, 

present no ohvious affinities. They cluster in an 1977; Bremer, 1991) placed it in Carlinlnae, and Petit 

isolated position ^vilhin Carduinae, in both comhln<Hl (1997) was the first to suggest Carduinae. Species of 

analyses, wnlhout statistical sui)[)ort (Figs. 2, 3). three of the geneia of the group {Chardinia, Sicbera, 

Eerardia was ranked among Mutisieae on the basis of and Xeninthemuw) are amnial colonizers of arid and 



characters (Dittrich, 1977) and we agree In 

waste-land thoroughout the Mediterranean region. In 

that the pericarp cells, with thickened u-sha|)ed contrast, species of the dwajf shrubby g(aius Afnpho- 
walls, are very similar to the ty{)e found in ricurpos are narrow mountain end<Miiics, sisler to the 
Cochnatiinae Hendh & Hook, f, a sul)tribc of rest of the gen(Ma of the Xeranthemum group In all the 
Mutiseae (Dittrich, 1996a). Furtht-r support for the, anal\ses (Figs. LA, 2, 3). 
albeit weak, relalionshi[> between Berardid and 
Siaeheliua is that the pericarp of Slaelielina is also 
''gochnatioid" (Diltrich, 1996a). However, we cannut 
state wliether this similarity represents conv(M-gcnce 

THK ()M)I'<}I<})IM cnOLV 

The usual tlefinition of this group is based on the 

or is a very oUl cliaraeter ((mserved in these two absence of receptacular bracts. A pitied, naked 

receptacle is olhtMwIse rare in the tribe. However, 
not all llu; st)ecies of at least one g<'nus [Alfredia 
Cass.) show an epalcate receptacle. In addition to this 

anomalous genera. 

Siaeheluia was previously placed among Carlininae 

(Bentham, 1873; Hunmann, 1891; Diltrich, 1977; 

Bremer, 1991), but Petit (1997) proposed moving it to character, aclicnes are also peculiar with pericarp 

Cai-.hiinae. For Dhtrich (1996b), Uie two species of diversely pitt(^d, wrinkled, or nigulosc (Su.anna & 

///msY/ F. and S. Garcia-Jacas, In press), but seldom smooth [Olgaea 


lohelii DC.) should be cdassiflcd m a distinct g(mus, and Syreltsehikovia). The grout) l^^s considerable 
Hirlellina Cass. All our analyses grouped llie included 
s[)ecies of StueheUna (five out of eight) in a robust 
lade with veiy high sup[)ort (IT - 1.00, Fig. lA; BS 


negative importance, because species of Onopordinn 
include some highly noxiou.-. weeds widespn ad in the 
Mechlerranean region and the American west like 0. 

100%, DI 



analyses ( 


ed ihe genus into Iwo well- 

34, 47, Fi^^s. 2, 3). However, both acanihiuin L. and 0. nervosum Boiss., giant thistles 

that can reach up to 3 m high. 

Three genera not included in previous slu(hes, 
Lamyropnppus, Olgaea, and Syrell.selukuiia, are 
classified in ihe Onopordiun elade in all three 
analvses, which confirm the group as a natural one 

sup|>orted cladt^s that coincide with Stnehelina s.s. 
and Hirlellina (Figs, 2. 3). which is compatible with 
the division of the g(Mius. iNeverthelcss, morphological 
differences other tlian [)resence or al)sence o 

f acl 


pilosity are virtually non-existent, and we prefer Lo with sig^rnficanl snpporl^(PP 
keep a single genus with Slaehelina and Hirlellina 91%, 9i%, DI 

1.00, Fig. lA; BS 

recognized at sectional rank within Si 
(Susanna & Garcia-Jacas, in press). 





In a previous study, the Xeranlhemuw group 

6, 4, Figs. 2, 3). Syreilsehikoria had 
b(M-n pnniously jTaced by Diltrich (1977) and Bremer 
(1994) in Centaureinae. Its classification in Carduinae 
and its relationship to the (Jnopordurn group was 
reported by Susanna et al. (2002) on the basis of 


Generic definitions In the group are unclear, with 

(genera Amphoriearpos, Cliarduua Dt^sf., Siehera, the only exception 

1 /// 



and Xeranthemum) uas placed among subtribe a polytomy with hnnyropappus^ Olgaea, Synurus lljni. 

Echinoplnae. lliis unexpected result led us to propose and Syreilsehikoria (Figs. ] A, 2, 3). 'Hie inclusion o( 

that the veiy small and peculiar heads of the genera of more species of Olgaea, which comprises some 15 

the group, with very large receptacular bracts, could taxa from ihe Tien Shan mountains of Kyrgy/stan and 

constitute a syncephaly (Garcia-Jacas ei ah, 2002). Tajikistcin, and its .strange relative Takeihulzurhia 

Our new analyses slunv that this view was erroneous Kitag. & Kitam. fiom Mongolia, may conlrd)ule to 

and, in fact, Harris (1995) had alrt^ady demonstrated a better definition of the gen(Ma in the group. 


Annals of the 

Missouri Botanical Garden 

Till-: {:\}a)i [s ckoip 


I 111 or 

s rrprrsciits a lar^r coinplcx of vcia spiiiN planl.s 
\>hicli arc usually callfMl llilsdes. All share inctlii 
large-sized heads, spiny leaves, auil a lun-^ papj)us 
delaehahlc as a single pieee. Our results indieale ihat 
a large lumiher of llie genera {Cunhuis L., Cirsiuni 
Mill., Notohasis (^ass., Picn()n}()ti Adans., Silyhun) 
Adans., and Tyrinmus (^ass.) h)iiii a natural gi-oup uidi 
signilieani parsiniony su|>p()rl (HS ^ 91%. I ()()%, 1)1 
= 10, I I, Figs. 2, ?)). Rtanaiiiing geiK^a, Cyuara L,, 
CiiUicl'Ucs iVIoeiieh, Laniyiopsls (Kliaradze) Dillrit:h, 
and Pnlostnnon Cass., are also plae(M:l in this group in 
all analyses, hut this is onlv supported Itv \\ 
Hayesian analyses (PP = LOO in all die eases 

Figs. lA 

sequonees (Susanna el aL, 200:5). The results herein, 
ineluding the fn)].-frnF region (iMgs. 2, ;5), do not 
ehange our pre\ ions main conclusions that die limits 
of Aniiuin L. and Coiisinia are imelear. Our stud 


(Susanna et a!., 200:]) demonslrated two principal 
e]ad(\s in [he Aniiufii group: the Arelioid clade 
supported only hy the two comhi ned analyses widi 


85%, 100%, Dl 

5, ;, I'igs. 2, 3) and die 

Cousinioid elade (snpj)orte(l by all three analyses with 


0-90, Fig. 1 A.: 13S - 92%, 94%, l)[ 

4. 3, 


2 :]] 

As [)ointed out hy Hadner and Ih'lluig (1999) and 
Gareiajaeas et ah (2002), ph\ logeuetie relationships 
and generic boundaries within the elade are obscur(^ 
(Fig. lA, 2, 3). One of the reasons for this is thai die 
co-e\isLeJice of annual or biennial species (most of 
Carduus, l^.dUirtitcs, Picaomon, Silyhum, or Tyrlmnus) 
together with penauiials (many (Cirsiuni. Cvf/ani, 
f/nnyropsis, and Plilosfcmon) huulers the assessnienl 
o( the two asp<H-ls from a molecular stand|)oiiit. 
Dillcrcnces in mutation rales between annuals and 
])(^nMinials (Caul el ah, 1997; Laroche et ah. 1997; 

Figs. 2, .'5). The Iwo groups can he segr(^gatrd by 
molecidar, chromosonu-, and pollen characters, but 
lliis grouping Is not conslsleni \Nilli moi'phology: Iwo 
genera of the grouji. Schnnilhaiismid C. W'inkh and 
Hypanmdnufn Juz.. are afTincd Avith Arcliinn on tlie 
basis of pollen, chromosomes, and DNA secjuenee: 
(Figs. lA, 2), but in other respects are morj^hol 
cally much closer to Cousinia. In addition to an 
Arelioid sjiecics grouj:) \vithin Cousinid, there is also 
a (Cousinioid gi'oup seen in \nlium. More sam])llng of 





* * 

ie oi)S(aire Lou.siiiki. subgenus llypaaiiilliodcs 
Tschern(;\a from Ctaitral Asia is re(iuire(h but it is 
highly probable that all four g(Miera udl have lo be 
grouped In Arcliuni. 

I^^inally, oiu- ITS analysis (Fig. 1 A) confii-ms ihat die 

pnr|>ortcd genera Auura and Tiaronirpus. as 


\iously proposed by Susanna and Garcia-jacas (in 

Amlreasm & Baldwin, 2001) make romparisnn of p,,,,,); ,,,„,„„ ,„. ,,_,,,„,) ,-,.,^ Cousinia\ 

DNA S(M[U(Mie(^s a less ndlabic tool. In (ael, un- 
cx|)ecLcd rt'sults, like the strange position of die 
annual genus Gabuiites, could be a result ol' these 

o w 



die) arc united with good support (Pf^ = 1.00 in boll 
eases, Fig. I A). 


dincrcm-es; Gahiclilcs is placed (dose to the base of 
the ihisdes in die combin<Ml analyses, gi'ouiKMl with 
Piiloslciuon (Figs. 2, 3), th(a-ebv contradict Inj 

Till-; SAiSSiUFA {,]{[){ I 

g mor- 

The ordy g(aiera phic<'d in the Sdussurcu group by 

l)hologlcal evidence [Culiirliles is morphologically Susanna afid Carcia-Jacas (In press) ihat w<M-e not 

snnilar to Cunluus or Cirsiatn). Ijiinvmpsis. the only imduded in om" previous studies arc Doloniiaea and 

genus i>r the thistles missing in our previous studies PolyUi.xis. The ITS atid the combined ITS + //7/L-//7?F 

arul seciuenced here h)r the first time, appears r<-]atcd analys('s jdace Polyhrxis basal lo Saussurnf with hi<^h 

to PliJiKslcmofi in the combin<'d analyses, without Hayt^sian (FP = 0.99, Mg. I A; PP 
support (Figs. 2, :]). Species of LainyropsLs have 
den late-spiny leaves with verv j)romin(Mit 




1.00, Fig. 2) and 
ooil parsimony su|)porl (BS = 87%, ])l ^ 6, Fig. 2). 
Bectanse S[)eries ol' Polyiaxis ai'c tlu^ onl\ annual laxa 
benealh. similar lo many s]ieci(^s of Ptiloslcfuon . The in this (dade, its l)asal position could originate in tlu 
affinities biMween die two genera wei'e pointed out by fasUn- evohilion of antmals ndative lo peixamials (Gaul 


Dlllrlch (1971). 

et ah, 199^; Laroche et ah, 1997; Anthva^ 

ai ev 

Taking into account our low sampling for such an Baldwin. 2001), in the sanu 





enormous group (ca. 500 species in total), any 
cotKduding remark on the thistles would be pie- 
maime. Tlie Carduus group, together with the Iwo 

Acumholepis always a])j>ears basal io perennial 

Erhinops (Fig, IB, 2, :5). \\\ its side, Dolomiaea is 



■ouped uilh high snpiKHl (PP - 1.00, Fig. I A; l]S 

OllOW 1 flii 

g ones, rf^([inrcs a more comprehensive 


94%. 1)1 

molecular analysis. 

- 6, Fig. 2) in the ITS and the combined ITS 
and //7/F-//7d'^ analyses with Froloria {Saussurca 


nil-: ARcncM i.koi v 


s group has been ihe subject of a recent 

(ishukinii lljiTi and .S. froforii Fed(d>.). It 

c(iualc lo consld(M- Frolovia, a genus restored b) 
Raab-Staube (2003), a synonym of Dot 



Another la\on thai \\a> not iiu luded in < 

mr prmaous 

pivliminary molecular survey, using FFS and malK study is lla^ purjiorted genns Aegopnrdon [Jurinca 

Volume 93, Number 1 

Susanna at al. 
Cardueae (Compositae) 


herardloides (Roiss.) 0. HoiTm. in Figs. liV, 2), which, 
accurdini2; lo Susanna and Garcia-Jaras (in press), 

tlie Rhaponticiun VaiU. group uitli Ihgh suj)porl (BS - 
85'^r. DI ^ 5, Fig. 2). Difficuhics in interpretation of. 

should he considered a synonym of Jurlnca. The even apparenllyunamhiguous, characters consistently 

conihined ITS + IrnL-lniF analysis (Fig. 2) place it in 

occur in Irihe Cardueae: as we liave seen ahove, the 

a rohusl clad(.' (BS 


91%, Dl = 1) ^vilh Jurinca naked receptacle is a supported character of the 

Onopordiun group (Susanna & Garcia-Jacas, in press), 


idered a distinct genus [Oiilreya Jaub. & Spach) hul there are many exceptions. Epalcate genera are 

ihat we m(M-g(Ml in Jiiriuea (Carcia-Jacas el ah. 2002). present in almost every 

subtrif)e: Tugdrinoria in 

ur re 

suits confirm ihat the limits het;ve(>n ,///n"//m Carlininae, Dolomiaea and part of the Onopordum 
and Saussured are not well estahhshed (as [nMuled out groni> in Carduinae, and Myopordon and Riissowia C. 

recently hy Kita et ah, 2001), because some species 

Vi'inkh in Cenlaureinae. To verify the ])osillon of 

formerlv Included in Saiissurea are grouped in ihe Myopordon within Centaureinae on morphological 

genus Jurinca (Figs. F\, 2). Saussurca carduinphala 
(lljiu) Iljin and S. dcltoidea (DC.) Sch. Bip. were 

grounds, the characters of the achenes are critical; 
lunvc^ver, we were unable to find herbarium matej'ial 

considered by Raab-Slaube (2003) as die distinct with mature fruits. Mouterde (1083) described die 

genus Hunahudla. Saussurca ceratocarpa Decnc. ^vas insertion areole of the achenes as oblique, a character 

for Raab-Staube (2003) a restored genus Upschiiziella. of Centaureinae. Tins observation contrasts with dial 

Both |)urportcd genera form a robust clad(^ in ihe I'fS of Wagenltz (1958), who reported the insertion as 

and the ITS + //7d.-/n;F analysis (PP = 1.00, Fig. lA; straight, which therefore points towards Cardnioae. 

Nikitinid was described in Carduinae. and in recent 

f the tribe was maintained In diat subtribe 

revunvs o 

13S = 98%, 1)1 = 6, Fig. 2). According to tins result, if 
we grant the genus levtd to this clade, U'umdaiclld 
should 1)0 consi(l(^red a synonym of Lipsrhilzielld. (Dlllrich, 1977: Bremer, 199d). However, achene 
However, we preft^r to consider it a synonym of characters arc undoubtedly cenlauroid (es[)ecially the 
Jurinca, because both pinported Himalaiella and double pappus, ilhistrated in Susanna et ah, 2002) 

and relal<' it to the genus KUiscd Cass, as confirmed by 

IJpsclntzicUd h)rm a monophyletic clade wilh Jurinca 

s. sir., with very high sui>port (Pi' = LOO, Fig. lA; BS molecular analyses (PP - 1.00, Fig. IB). 

= 100%, DI - 15, Fig. 2). 

No final conclusions can be drawn from Uus CoiNcriDING Rkmakks 
entanglement of genera, because our sampling of 
Jurinca was \crv limited. llo\vev(tr, a redefinition o( 


1 a 

more suitable out group and widi the 

the boundaries belwctMi Jurinca and Saussurca is additi<Mi of die //vdW/v/F region, die systematics of 
clearly required. The clarification of these hmils, and Canhieae now appears to be more fully resolved. 
inde(Ml die description of new genera in a complex in Howtn^er, diere are taxonomic issues that renunn 
which no less than 15 have been already descrilxMl unclear and llieir chu-ification requires better sani- 
(Susanna & Carcia-Jacas, in press), cahs for a much phng and more morphological and molecular data. In 
more com|)rehensive sampling than any performed lo addition to only moderate support for basal branches 

in the combined analysis of the three regions, doubts 
remain reganHug problems typical of delimitation of 
very large g(Miera such as are frecpiently found in 



Compositae ((dassic examples are Aslcr F., Erigcron 
Our results confirm die gmieral outline of CeiUau- \^ i)\- Scnccio F.). In Carduinae. generic boundaries are 
reinae proposed by Garcia-Jacas et ah, 2001, this time (hflicult to eslablisji for Citrduus, Cirsiunu Cousinia, 
on the basis of three regions of the genome (Figs. IB, Jurinca. and Saussurca, In the case of Carduus and 
2, 3). Here we describe only the most imporlanl Cirsiuin, (^xtensive sampling in Africa and North 
results, namely the inclusion of two genera h)rme'rly America is needed. For Cousinia, Jurinca, and 
classified in Carduinae, Myopordon and Ndiilinia, in Saussurca. which are the easternmost representati\es 

of the tribe in Eurasia, intensive collections are called 

the subtribe. 

Myopordon was considered related to Onopordum f,j,- i,. Central and East Asia. 
(hence the name) and [)laced in subtribe Carduinae 


)ecause o 

f the aljseiice of receptacular setae (Wa- 

genilz, 1958; Dittrich, 1977). hi contrast, the ITS 
analysis relates Myopordon lo the genus Oligochacla 
K. Koch of su])lril)e Centaureinae with very high 
support [VP - 1.00, Fig. IB), and the combined ITS + 
IrnL-lniF analysis [>laces Myopordon deeply nested in 

iJU'raluic (^ilcil 

Andrrascii. K. tK H. (]. Baldwin. 2001. Unequal cvolulionary 
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rDNA internal and external Uaiiserihed spacers. iVIolcc. 

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Annals of the 

Missouri Botanical Garden 

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1996. y\mong-site varialii>n aiu 

I its impact 

on plivlogcnetie analyses. 4Ten(ls Eeol. Evol. II: 367- 

Voliirnr U.'5. ^'unlh^■r 

l>p. 1-1/2 oC ilir An.\a[> [ii [i!K Mis.siJtKi RtnAMCM, C\Ki)i:\ 

was piil)lisli<'<l nri May 3J, 2()()f). 

Missouri Botanical Garden Library 

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Species Reconsidered: C()nsequenecs for Biodiversity and Evolution, the 50lh Annual 

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Species Reconsidered: Consequences for Biodiveisily and Evolution. Tiilruducliun .„_ 

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Liiuiaeus's Biolog)^ Was Not Essentialist . . Mary P. Winsor 2 

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Adaptation, Speeialiou, and r!(inv(ugence: A Hierarchical Analysis of Adaptive l{a<lia- 

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The Cardueae (Composltae) Revisitetl: Insights bom ITS. /r//E-//7/F, and mat¥. Nuclear and 

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llie 5 1 si Ajinual Systematics Syniposiiiin \\v\i\ at sperm l)i()g(M)gta(»liy and past continenlal m()\('- 
llir Missouri Botanical Cardeii, Ocloltcr <>— 1 0, 2004, incnis,'' in llic Annals of (lie Missouri flolufncal 

— Garden, Tlial paper did mueli In revilalize inler(-st in 


a 1)1 


()geogra|)ny and lo moaeriuze prev 



n^' views abonl 


had as its theme L(ain Ameriani Biogeography — 

Causes and Efjeels. The |)a])ers in this vohniie were 

either presented at the symposium or are iinited the pli\sieal e(nile\t within which these pattern^ and 

papers 1)) specialists on related to|)ics. The lad of 

all I HI ties oi'i<^ina[cd. It still resonates \\i 


200] was an appropriate time to consider [taltcrns of hecause it focused altenlion on two components 
plant and animal (.hstrihulions widiin Latin America essential to uncK-rstancHng the arrangement of organ- 
aiid dieli' aifiiiilies with oilier lands h(H:anse it was isms and communities over tlie lan(lsca[)e. One is die 

30 years ago, in the (all ol 1974, lliat liavcMi and need for a taxonomy that reflects distrdjutions that arc- 
Ax el rod puhlished their landmat'k pap<a,. "Anglo- hiohtglcaily meaniug(ul rather than ones thai are 

'This and the 10 atticles that follow il jtr llic piot-ectlint^s ol the ol^^l \iinual Syslemalics S) ni|)oslLiiii ol llie [\lI->outi 
]"i(>taiiical (Jai'dcii. Ldtin Amcnecu} Biagcj^igniphy — Causes and A//i"r/.s. 4hr s}tiiposinm was hrhl 8—10 Oclohcr, 2001 ii\ the 
Missouri ii(»lanieal Carrlen in St. hoiiis. Missouri. I .S.A. 

" This was ilic 1 9th Missouii Botanical (harden \Mniial 5s.itcniatit\-> S\ nlpo^iu^l lo he supportrd hv a jirant Iroiti ihe National 
Seienee Foundation (jiranl DEB-99[] 16 12 ). Vinon;^; I he inaii\ jx'rsons eoiilii hilling to llie planning and operation of I hi- iMeelinjj. 
and to ihc piiMication of the papers ai'c Olga Marllia Monlirl (Centoi" U)V Cotis{T\ alion am! Suslainahlc l)e\ olopnicnl); Mi<-k 

liiehardsori (He.seai'ch. Graduate Stndi<'s). \hna 1* reire-F lerro. ami Sandv Lo[>ei^; \ letftria Hollo\\ell (Director. Missoin'i 
Bolanlcal (iardeii Press). Carmen I Iloa L Iloa. Ann McPhorson. and Bclh l^arada: Donna Miller and Znhiii (]liandi"ati 
(hJonnalioii Terhnohjgy); A^'ilham iW\y (P'a( ilil\ !Sii[)poi"t); and Mar\ McNainara (registrallon). 4liib syniposiiim, together wilh 
IV\ pro\ ions on(\s, again henellled considei"al>l) from llie <'onliil)ulions, suppoii, and oncoin'agenient of Pt^tei" Raven. 

■'This syriiposimii Mthimc is dechealod lit P.arhara W. Piwdon, onr esleerned colleague and an invited speaker lo ihc 
Synijjosiiini, \\ho died in Peljriiary 2()()f). SIk; eslahlished herscK as an nnp(n1anl conlnhiilor lo QuatiM'nai\ veg(^lalion liislorv 
and palcoeeohjgv ihrougli papers on rapid climate cTangt^ and pet lods ol arid] I y at glacial-interglaeial houmlaries in 
Gualemala and in the Lake Valencia Hasiii. ^'emv.neIa. Bai'hara gained lurlhei" inlernalional re|)utation and respect for her 
laW'i- work on the (^niromnents of the Low lami Ma} a region of the Yucatati Peninsula and adjacent Central Atnei'ica. W e join 
wilh onr editor \ icloria llollow(dl in celehialing hei- ciilical and hroad-hased experlise and liei- \ihrant contrihiilions lo ihe. 

' 1 lit: editors of the Aiuuds ihank Sophia Halcomh for lit.'r significant ethloi iai eonlrihulion to these papers. 

■'Missouri Botanical (warden, P.O. I^ox 2'/), St. l.ouis, Missouri 63166, U.S.A. ahui.gialiani(?^^mol) 

Ann. MissoPHi lior. Gard. 93: 173-177. Pi blisiiki) on 23 Apcist 2006. 


Annals of the 

Missouri Botanical Garden 

arlifac'ts of iKunciulaLure. Y\\r other is the ikhhI for Aiiicrica and other lands u( [lie Soulliern Hetnisplicro. 

sound inodeU ol hmdseape e\()liilioii and einii'on- Secon(h to dociitneiit some of the (orenig tiiechiuiisnis, 
nietilal ehauiie as a context (or reconslruelin^ especiall) plale teelonies. land hrid^ies, and iditnatiL' 

change, dial help explain f<)rrner distTihntions and 

migrations through time. 

An onlgrowth ol this revitah/alion in l.)iogeography tlieir residual |>all(4"ns in the modern biota. Third, to 
has been the application of new informalion and show llie variely ol melhodologii^s now avaihible for 


analysis from niol(H'n1ar biolog) (phylogcograph)) to 


document nig these forcing mechanisms and their 


s. Tl 



ogieai consequences, i ne most enngnuaiing o 

these methodologies oft(Mi comt^ from on I side die 

biological sci(Mices and include salellite imagery o( 

augment and test long-standing knowhMlge derived 
fi'om traditional a p[) roaches. There are now more 
accurate and temporally exact uutdels of philc 

Leclomcs (PIndell, 1994; Pindell tK Bariett, 1990; attnospheiic events; recejit ifnuuations In quick-time, 

Mann, 1999), and there is a bettci' appreciation ol its detailed, multi-factored [)aleog(H)gra[)liic comj)uter 
conse([ucnces, incduding die direction and rates of animations (Scolese. 200 1); geochemistry; geo])li\'sics; 

marine sedimentology; and the myriad of factors 
determining weather and loiiger-tei'm climate. Rela- 
tionships between seemingly (lis])arate obs{M'\ati()ns 

are a rich smin-e of new Insights into biogcographu: 
problems unn^sctlved by traditional approaches. To 
this end, a hjurlh goal of the symposium was to bring 
toirether speakei's not tradit ittnalb part of a siiiiilc 


crustal mo\cincnl, the reconstruction ol lan(_l 1 

the uj>h(t of mouiilain systems and plateaus, and thi 

partitioning o( [)o[>ulations by changes in draiiiag( 

systems. Tlua'c is also an expanding paleontologica 

basis for traiing the elfecis o( these events (»n the 
distribution ol lineages and communities and an 

increasing a\Nareness of the 

impressi\ e ai'senal of 
techniques from iiidef)eiid(Mit disciplines now avail- 
abb; lor reconstructing en\ Ironmental change and the 
biotic responses (see below). 

Also Iinpcjrtant. but still in the formative stage. Is 


I. : 

gathering to discuss results from diverse disciplines 
relevant U> bi(tgcography. 

Consistent with these goals, the discussions begin 
with a summary of the; biogeogra[ihic liistuiy ol 

development of a database o( fossil [)lants ihat rrondwanan \ertebrates by David Ixrause and others 
j)ro\ides a more (*omj)lete and reliable checklist o( and a lil>torical |)erspeclivc of South American land 
taxa and their age. Identillc-ations of rTiegafossIls In tin; mamiiials by Rosendo Pascnah The next papers focus 

on develo|>ment of the land bridges that connect North 
and Sinidi America and the history of miurations 

across those brid^res. E\'ohitionarv biologist Rlair 
Hedges smiiiiiari/,es current tli inking about the 

older literalure :\rr notoriously unridiable, as ai"e many 
ol the bn»logical altnuties c,it(.;d in stratigraphic 

palynological publications for (a"etac(M>us and (^(mio- 
/.oic plants. It is incom|)rehcnsible in this modern laa 

that key liiformat ion for fossil [)]anl remains is so evolution of die West Indian \'erl(d)rate fauna within 

tliat [)h}.^lcal conl(^xt, ami S. Da\id Webb reviews the 
(keat American Hlotic [nteri-hange, bringing a lifetime 
of experience to intcipretlng the complex events that 
led to the formation of the Panamanian land brldire 

inaccessible. These data are badi 

led f 

} nct'dcu lor dating 
[jhylogemes, c:ald)ratiiig molecular clocks, and con- 
ducting studies on vicarlance and dispersal. They arc 
also valuable as historical background for forimilatiiig 
speciation models and ni making paleoen^dronmental 
reconstructions as analogues for the (effects of current 
enviromnental trends. The onliiu' (dectronic frame- 55 million years of separation, 
work for such databases aln^adv exists, but 

and to documculitig the 



conse(jU(Mices o 


the union al South \inerica with North America aftei 

a co- 

More rcct'ut cveiils and the biotic responst^s that 
ordinaLed effort by paleobotaiilsls wiM be rctiulrcd to moderiii/ed th<^ landscap(\ environments, and coin- 
lilter into the system more complete records assessed munities of Latin America in the Qualernar)' are 
loraccurac). discussed in three paj^ers. Sarah Metcalfe reviews 

The new analvlical tools available, and the novel information from spores, ])ollen. diatoins. r(K]ent 
concepts being generated, are ]")art of the reason for middens, dendrochronology, and ih^ep sea cores l(j 

reconstruct fluctuations in climate for the northern 
three major symposia <levoted to the subject within the deserts and the central Transvolcainc Ridt of Mexico, 
past three years — Tropical Inlcrconliiiciildl DLsjunc- 

Jiaicwed inler(\st In biogeogra[)hy. Then^ have be*Mi 

Allliough the record is com|)lex, Late Quat(M"nary 

lions, organized b\ Susamie Remier and Tliomas 


4 « 

events, (locumented initially for the high latitudes, are 

including a dry mid-Pl(Mst(»ceiu;, a more moi>t 
Holocen(\ and 1^1 Nino— Southern Oscillation (KNSO) 

Civnisli (200 1); Dispersal, edited l)\- shown to have affected northern and centj'al Mexico, 
Michael Cam. Ran \athan. and Simon Levin (2()()."5); 
and the [iresent volume. 

The goals herein are, first, to illustrate and update cycles. In contiast lo older views that coiiditioiis and 
present and past distributions for sine ral major groups communities became more stal)le and were essentially 

unchanged toward the tropics, a wealth of cv idcncc 

ol organisms, with particular reference to Latin 

Volume 93, Number 2 



now (locumeiiLs that tlie clirnales and l)i()las al llic pollen record ihaL llie genus fnst appears at ihc 

lower laliludes had a dynaiiiir and complex (^ualer- middle to lale Eocene transition (ca. 45 million years 

nary history. ^^g*^) ^md has been more or less continually present 

Human influence IxH-omes a factor in shaping the ever since. One inteqjretalion of the emerging 

[notas of lowland Central America by 20,000 yr. I5P, molecular (;\ idcnce is that, rathi-r than distributional 

ami that history is recounted by Dolores Piperiio using and taxonomic sta'sis, the genus disap]>eared for an 

plant microfossils, charcoal, and, innovatively, a group estimated 3 million years between ca. 14 and 11 

of plant crystals called phylobths and starch grains of million years cXgo, and that die modern black 
agriculturally important plants presented on grinding 

One long-standing l)arricr to the detailed recon 

mangroves are derived from i)rog(Mhlors that arrived 
ca. ii million years ago. Il is [possible that both 
results are valid because the stenopalynous pollen 
slruction of Quaternary vegetation hi^tiny Ironi high establishes the {presence of Rliizophora, as a genus, 
alliludes in the tropics has been the lack of continuously in the region for 45 nullion years, but 
continuous or near-continuous records. Cores from does not preclude the extinction and re-introduction 
which paleobiological information on terrestrial l)iotas of the molec:ular-defined extant lineages throughout 
arc retrieved mostly extend back only to a|)[)roxi- this intervab A duality of stasis versus more dynann'c 
malely 60,000 yr. BP or less, and rarely into the change w III likely become commonplace as paleobio- 
previous intergkicial at 100, 000 yr. P)P. Tln> means geographic pallerns and evoliilionar\ histories Irom 
that records nmst be spliced together fnjm dinerent the fossil record and from moUnadar data are 
sites and studied through a variety of lechnicpn's. The compar^Ml. 

results have been ]ess-lhan-con.-5istent acct)unts of th( 

Mv other contribution involves a synthesis of 

climatic, biotic, and uplift histoiy for several r<^gions observations Irom dideienl discijilhu^s regarding the 
of the Nootropics (e.g., the Atacama Destai and the increasing mmiber of elements that are recognized as 

having migrated between Africa and the Caril.)bean/ 
South American region. This interchange has been 

high elevations of Chile and Bolivia; Grosjean (;t al., 
2003; Raker et ak, 2001). This limitation was removed 
(or one site in norlliei-n South America when cores 

lislied i 



accom[)nsne(i \\\ a variety oi wa)s, uiciu(ung vicari- 
dating to L6 million and .'5 ance in Cretaceous and Paleocene limes, expressed 

primarily at the higher taxonomic categories; dii'cct 

357 in and 586 m long, ^ 

million years, respecll\c]), were drilled through 

sediments of the inl(Mandean basins around Pxtgola, 

Colombia. These coi'cs \si^vv obtained by a grtiup Irom 


overland migration across the North 
bridge mil 11 about the middle Koc(Mie; 

\tlantic lanil 

and long- 

the University of Amsterdam and their Colombian distanc(; tlispei-sal occurring dn-oughoul this time but 

becoming essential after about the middle Eocene. 
The relativ(^ importance of thes(; ovcrIa[)ping modes 

coljeatrues led bv lleniT I htodiiemstra. The histor\ ftf 



montane veg(^tation is reveal cu in 


considerable detail from Funza, and these and othm- depends on the dispersal potential of the propagules, 
studies in the northern Andes are re^■ealing abrupt, 



the ecological reipiirements ol the nngrants, tlie tmie 
during whicii the lineage under considiaalion has 

short-term fluctuations in climate such as the Little 

he Age, Younger Dryas, Heimich, and Dansgaard- been in existence, and the physiographic and climatic 

Ocschger events long recognized In sediments ftom 

the Norlhern Hemisphere. 

The fullest understanding of tropical ecosystems relc\'ant to long-distance dispersalbetween Africa and 


conditions pixnainng in 


the region being transversed 
at the time the migrations occurrtuk Observations 



recpnre a seamless integratmn of :!.Ludies on their South America arc: (1) the enoiinous quantities of dust 

and organic debris being blo^\Ti from the Sahara and 

Sahel into the Caril)bean reiiion, especially diu'ing 

histoiy with those on the existing temporal \'ersions. 

This svnthesis has yet to be fully achieved, but tlicn^ 
is some information on the Quaternary Allanlic Forest periods of major hurricanes; (2) lite increase in 
of Brazil (Ledru et ak, 2005). This will comjihaiuMil huiricane intensity, and possibly hurricane frequency, 


widi global warming; and (3) the existence in 

nicely the studies of Hodolphe Spichiger and others 

(e.g., Perret et ak, this volume) on the biogeographic geologic past of intervals wh(Mi global temperatures 

histoiy ^)f the Cesneriaceae in the Atlantic Forest \Ia were con>idcrably warmer than at j)rcsenl (e.g., during 

dispersal-vicariance anal) sis. 

the earlv Eocene climatic optimum and in the middle 

M) own contributions on the geologic record of the Pliocene; Schmitz et ak, 2000; (^ronin & Dowsett, 
Rhizophoraeeae and on the origin of Abicau-Scjuth 1991). Fujihcrmore, the Eocene was the lime of 
American l>iolic affijiiti(^s make two points not widely 

emergence of the Greater Antilles, and the distance 
between Abica and South America was about one-half 

emphasized in the current bi(jge()gra[)liic literature. 

With reference to ihe hisloiy o{ Wdzophoni in the to one-lhird h;ss dian at present. Thus, the opportunity 

Caribbean region, it is clear b'om the extensive^ fossil for wind transport for some organisms and/or their 


Annals of the 

Missouri Botanical Garden 

prn|")agiil('s mixy hiwc l)eeii gi'enlei" (liii'ini^ these |)e;iks 
(if wainitli lliati would seem plausihle iiii(Je'r luotleiii 
eonditioiis. There are exlaiil plaiil genera in which 

* « 

s 1 

a\allalile lor iii\ est Iga ling llie historical aspects of 


list aiiiiiiienls tl 

le loiiowang list augments me a])- 

eeosvstenis, tl 

proaches noted in the |>apei's of this \olutne (see also 
( waharii, \^)^y): chaplei 4 — Methttds, Piinclples, 

Slrengdis, and Liniilalions): 

(i) It IS IKJW jutssihlf I*.) (IclnriiiMc llic cuneeiiliatKHi of 

CO-? iind olln-i" "■I'eonliDiHc passes Iti lh<- I^'arlli's 

— O o 

atMi(>s])[ir]-c {)\{'v tli(^ past 100 iiiillinfi \cars. (■ori'cjalc 

tile fliii tiialioa^ w itli U'liijK'iaiuir lrcn(l> lia>('(l on 
oxygen isolojx' ratios, dale th<' e\ents tln-ougli 
palrcjinagnclic and hiosLraligrapliic stu(Ncs, and 
relate ihc rcconshnieted cliinalc to the hisloiy of 
hncagcs and coaiiianiilics. Tins is aceoinphslKMl hv 
.siicli diverse tcehni<|ncs as aiuiK/iiiii iras m aii" 

hnhMrs ti-appcd in ici' and hv cahulaling tlu- 

\\\ ici' ami 

C'liaiigiiig ina» ol the I'^aiiirs carhtjiiate sed itiuail: 



thi'ongli hmc. It is also possihir tii rallhiatr ihc 
sininalal indc\ of leaves from extani plants gi'ow nig in 
cm ii"onnn-nls ol known (iOo eoneeiilralion. as well as 
fi-OMi iH'rhariiini sIteeU. and lo ap|il} the Indiees {a 
io^sil (aitieles of diliereiil ages. Iw this wa) , pa^l 
eoneentral ions can he eslinuUeiL and the fluetnalions 
can he eoin[iar*ed willi leniperaline trends horn 
o\)gen i>olope ^ladies in die marine realm and uitli 
vegetational liislories from llie terrestrial en\i!()ii- 

Changes in alhedo (refl<M'li\ itv). pr(vipitalion. earhoii 
storage (sinks), and earhon reh^ase (pnm])sl can he 
estimaled lor \ariou.s \c'gelahon t\pes (e.g.. Mindra. 
hoixvil r{>res!. hopieal lain (oresl. tropical sa\anna.s) 

and die elimalie im])neatiori assessed as \egelalIon Is 

(deared or as one \'egela!iori I\pe (e.g., lowland rain 
for'csl) IS repLieed hy another (e.g.. eaalni^as/eerrado) 


. Mi 


o\('i" geologic lime, /\lteratlon^ in plant comm' are an 
iinpin'taiU h'edhacT lo climate hecause, for example, 
luiK o( die piccipitalioii o\ cr the rain forest is 
generated h\ die forest itself ((dappcrlon. 10*^.'^). 
The anion Ills of insolation ean he eahm I at cd fur 
.specihc plai'i's and tunes as tlic Ktirdi chaiiLics 
posilion relative to tlu' sun (die Milanko\ itch c\( les). 
It IS also known dial tin* solar eonstanl (2 cal/cmV 
min) has varied o\ (m- linn-, and although these 
lluclnal ions eannoi he preciscN^ (fnantihed am 
not s<'em In \ ary in e<incert \\ llh eviniel lous. 




molecular e\ idenee suggests (lis|uuetions between 
Old World ami New World hixa originated ca. l\—l 
niilliou years ago (viz., in the middle Pliocene; 
(iraham, tlii^ \ohnne). 

C]olleeti\"el\% tln^ ])apers of the sN'tnposium ilhislrate 
some ol the j^ast and [iresent chaiac-teji sties and 
alliintles of tlu^ Latin ,\m(n"ieaii hiola and the i'ans(^s 
leadnig to its modernization. Interwoven tlironglioul 

ar(^ examples (d ihe various teelmi(pies Ixdng utilized 
to reveal their history. IT is recoid is Ixuaaning 
iiicreasiuglv i'(M*oguize(l as impoitant to mitUastaiiding 
the origin, (le\'elopm(Mit, and fimctioidng of tlu^ 
|)resent (annal and florist le eomniunities and In 
anli(dpaling future eiiviroinn(nital and Itiolie eliange. 
To emphasize the eonsid(?ral)le array of teehnltpies (5) 






c\oliilionai) peaks, or iiiigralional histories, th<'y 
(Minsliliile a dam]ieiiing oi- amplilving overlav In the 
iM ilanko\ ileh \ aria I ions and odier climale-lorcing 

The hi 'I gill of monnia I ns a I \ arions points m I nne can 
he est una led In cahailalinir the mean annual 

le ahinide of the highland flora 

lempiMatnre ol [ime-e(|ni\ aleiil fossil floi'as Irom sea 
level and Irom hiiili elevations nsins: the modei n 
analogue method and/or leal maigln aiuiKsis ((w'e- 

gorv-V;od/i<-ki. 2000: Graham <-t al.. 2001). IJy 
afipl}iiig tlu' average glohal lapse rale ol (!/km, 
an appi"oximatif>n ol t 
ean he made. These eslimales. toiretlua" with other 
geologic information, liave r<'\ealed that a])oiil hall 
the cl(wahon of the Central \iidcs has hccii attainetl 

in rehiUvciv r<'cent times (viz.. since the hUe 
Miocene). 'ITal has implication^ lor such topics as 
the time of origin of p;irarno cnvii'omiients and 
vegetation. s[)ecialion f>v vicarianct; in the region, 
and the migration of ttaujicrate and lnt:h-altini(h- 
oigamsms along die axis (tl du 


ligh Andes. 

TIh' growth ol stalagtil(\s. and the midges and mites 
tlicv oltcn contain, is ln-iiia used lo estimate 
precipiladoti histca^ in die|-|s of die sou di eastern 
L'ni[e<l Slates, in adjacent uoilhei'ti Mexico, ami in 
Bra/ii (c.i^.. i'olvak el ah, 2001). 

Ammo acid raccmi/ation in ra<lioearltonMlale<l emu 
eggshell Iraginenis is a finichon (tl lem]teraliire, and it 
is heiiig used lo rceoiislinci eliinales In pails ol die 
Sondiern I lemisjiliere (Johnson et al., 1900). 

Alkenoues are long-chained oigaiiie iiioltMailcs from 
algae that preserve in oeean sediiiKails as hio- 
chemical fossils. The degi-ee of unsatnralioii is 
tempcianir<' sensitive (iiKacasing unsatui'ation indi- 

eali-s eooling water), and this afltads a method ol 
detecting Id [Nines during times licvoiid hishirical 
records. The modern cv (T' of K\ Nihos along ihe 
Peiaiv ian coast apjiears to have hcgun ca. SJUIO \r. 
iJP. and il correspontis lo a lime of intense incjiinmcnt 

JJl. anil il correspontis lo a lime ol intense incjiinmcn 
hnilding. v\ hile the onset of cv tai strong<'r ev cut: 
eoi-rcsponds lo tlu'ir ahandonment. 

The soliihilit\' [>f nohle i-ases is denendent on dit 

s dependent on die 


tempera I II re ol die water, and ' '(^-daled samph^s h"oin 
groundwalef in Hra/il indieale a cooling of .^ ('. at the 
I.ast (dacial Ma.xhiiiim ca. I'LOOO v r. Bl'. This is one 
example Irom a vveahli of new information thai 
indi<-ates lowland Amazonia cxpciifaieed significant 
cooling during the Qnalei iiaf v . \\ liedicr it also 
experienced di'ving and, il so, when, v\lua"e, and to 
what (~xlcnl, is still unknown despite [)roclaiiialions to 

V ^ I 1 <. 1 1 t \ I t III, 1 ,-> ,^ I I I I 1 1 I I \ I M M 

the eoiiMarv in ihc inin-h-< 
'11', ■ . ■ I 

I It; 

dialed issue of refugia. 

ic eoiinarv ni nc inin-n-< eiia c( issue oi rciuiiia. 
itaiiiiim is a terrestrial mifuaal that is found In ofl- 
lon- l)aslns ol \ eneznt la. Det rcasc.-' in the ainonnts 
ahaig scclions of marine cores I'eflect peraids of 
reduced riinolf and river ll()w. and it is one indication 
ol aridilv associated with coolin;^ in Amazonia durin 
inleiv als ol the Oualeruarv. 


Ceograplheal iiihainalion s\st(aiis (CIS) tools, n-- 

motelv' senseff dala, and in<'hi' modeling leelini(]ncs 

are heiiiii inn'iirated with holaihcal data lo sliidv the 


ecologv and evohitlon of [ilaiil geographic ranges ami 
spatial ])atlcrns of di\ (-isit) ('IVisha Coiisiglio. 
Analvsis I nil, Center lor ('onsia'v alion and Sustain- 
ahic Developmenn Missouri Botanical Cardeii; peis. 
coimn.. 2000). 

These and other te(Tni(pn's demonslrale how (ar we 

have come since the earlv gicat sxiilhtlie iniiuls ol 

Volume 93, Number 2 



biology laid llu^ foundations of biogeograpliy. bin- 
naeiis, tluoiigli llic lt>6 dissertations ot [lie Aniocnt- 
Idles Aatflrffilcdc, iioled tlial the vegetation of dislaiit 
regions sho\v(Ml florislic siniilai'ities (e.g., Kamchatka 
and easlern Noilli America in ihe 1750 chsserlalion of 
Jonas P. Flaletiins); llial is, there were pallerns in ihe 
arrangcMueiit of organisms over llie landscape. Von 
Himi1)oMt eslahlished in 1807, from tiis ol)servations 
in the Ecuadorian Andes, that vertical cliang(^s in 
eotnmunities along mountain slopes were compaiable 
to hori/onlal changes with latitude. He co?icluded thai 
climate is an im[;urlaul factor hi (Jetermlning these 
paHerus. and dial did much to place the study of 
hiog(M)graph) on a scientific basis. More recently, the 
eonsidei'alion of time antl the occurrcju^e o( [lasl 
events has become increasingly recognized as an 
essential component of bi()geogra|)liy, as it \\as whtMi 
geologist hyell irnphmled the concept that lineages 
and coinmuiiilies extend back lln-ough liuK^ in the 
thiukiuii of Darwin and Wallace on e\olution. The 
papers pres(Miled here, and in other recent symposia, 
are a stalcmcnl of the progress beiuir made in 



1 tl 



n g me can ses and me im| > 1 1 ca 1 1 o n s o 
plant and animal disti'if)uti(>ns. The likes of IJiniaeus, 
Von Ihnnboldl, Darwin, and Lyeii would undoublcdiy 
be amazed and immensely pleased.<Talin"t' (iilcd 

Baker, I*. A. ct ak (+ 8 autlidrs). 200]. Tropical ciinialc 
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Cain, M. L.. K. Nalliau tX S. A. Levin (cdiloi^). 2002. I.orig- 
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ot^V oi Soul 1 1 Anirrica. Elsevier S('i{aiee ^^ 


Cronin. T. M. iS. 11. .1. Douselt (editors). 1991. Iliocciic 

climates, (^)ualfin. Sci. Kev. 10: 115-296. 
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North Xmi'rican V^-gclation (Nortli of Mexico). Oxioiil 

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(iri^i3:on-\\ (nl/ieki. K. M. 2000. Li)lirt hislor\' ol llie eeiitral 

and norlhern Andes: A re\iew. I3nll. (/e(tl. Soe. .Vnier. 1 12; 

1091-1 lOfx 

(yrosjean, \L, 1. Cartajena, M. A. Ge}h i!^ L. Nunc/. 200-"^ 
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Moloeene paradox of the Atacama Dchcit, northern Chile. 

l'alaeo<i;i'o<ir. Palaeoeliniatol. Palaeoeeol. 194: 24w'-2.'>8. 
Haleiiius, J. P. 1750. Planlae llaiiores Canisehaleenst^s. 

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Johnson, H. J., G. H. Miller, M. L. Lo-eL j. W. Ma-ee, M. K. 

(/agan & A. R. (diivas. 1999. 65.000 years ol vcgctalion 

I'lian^e in eenlral Australia and the Austialiati summer 
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Ledru, M.-P., D.-]^. Rousseau, F. W. Cruz, Jr., C. Hieeomini, 
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(luring the last 100,000 \i from a record in llio Hrazilian 
AtlanLie raltifoiest region and inlerhenil>plieiie c()nipai"i- 
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Mann. P. (<'ditor). 1999. Carihbean Basins. Klse\icr Seienee 
I'uhli^lici's. Amslerdani. 

Piiidell. j. L. 1994. Evolution of the Gull" of Mcxieo and the 
(^aril)hean. P\). 13—10 in S. K. Dono\aii iS. T. A. Ja( kson 
(editors), (Carihbean Geology: An Introdnelion. t niversity 

of ihe West Indies Publishers' Association (L VilP.Vj, 
Viona, Kingston. 

& S. F. Barrett, 1990. Geological e\oIuli(>n ol the 

Carihhean region: A plale-teelonje perspeeli\e. Pp. 40. >— 
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Sotaetv of y\nieriea, Boulder, Colorado. 
P{4^ ak. V. J.. J. C. Cokendol[jliei", R. A. Norton tl "i . 
Asmeront. 2001. N^'^otler and cooler lair MoIoccik^ climate 
in the sonlhwestern United States from imtes [i[('ser\ed in 

stalagmites. Geolog\ 29: 643—646. 
I { axon. P. n. (.K D. L Axelrod. 1974. Angio>perm hii)- 

geograpliN and past eonlniental aio\enienls. Ann. Missouri 

lio!. (iard. 61: 539-673. 
Heimer. S. S. & T. J. (ii\iiish (oriianizers). 2004. Tropical 

intcr<-onlinenlal disjunc lions. InL J. Plant Sei. 165: 


Srlimil/, B., B. Sundquist & F. P. \n(h'easson (rdit'a's). 
2000, F-arh' Paleogene warm ctimales and hios|)liere 
d\ fiamies. 

Gf4-' (G(M>logieal Society of Sweden) 122: 


Seotese, C. R. 2004. Cenozoie and Mesozoie ]ialeog(^ogra|tli\ : 
(diaiiging lerreslrial biogeogiapliie pathways. Pp. 0--20 in 
M. V. Lomolino & L. R. FIean(^y (editors), Froiiliers of 
Bi(>jj,eogra[)li)', New Directions in llie Get)grapli\ of Natuic. 
Sinauer Associates, Sundeiland, Massadniselts. 

Von I limil)oldl, A. 1807. Essai sur la (ieographie des 
I'laiilrs. Levraull et Sehocil, Paris. |See also, hleen zu 
eirier Geographie der Pflanzen, Ed. Reprint 1963, 
\\'k^senst4iaftlie]ien Buehgeselfsehaft, Darmsladld 


Uaiid IF. Kr(Uisc,~ Pulrick M. O'Connor,^ 
KnsLina Curry Rogers,^ Scott D. Sampson/^ 
(Gregory A. Buckley,^' and Raymond R. Rogers' 

Ahsti; vct 

The Maliajaii^^a 15a.sin I^-ojccL initiated in I'^O:^ ii\u] ceiittacd in U[)p<a- (acLicroiis slrata of norlliwcstfrn Mad;ijj;;]S(';n\ lias 
icsnitfti In llu' disco\fi) of sonic ol l\w. rnosi tMiinjjltUe, \vcll-pivsci-ved, and hi^nifiraiil bpucirni-iis of Laic Ciclam^ous 
vci"t(^l)ralr aiiinKils imm the Sonllicni HriTiIsplicic and in<lccd llic world. Anion^ die mosl iinpoitanl finds arc various 

specnncns in crocodx liloi-nis, non-a\ian dinosain-s. and iiiaininals; dicsc finds lia\c llic pofcniial lo piovidc kc\ insi^hls inio 
die l)io^i-o^iaplii<- and paK'D^rn^fapliic ln>lor\ o( ( /ondwaria. Madagascar has hciMi plivsicalJy isolaN-d frnni Vfi'ica for ()\<'r 
160 an' I lion \cars and Ironi all odua' major landnia.^st;s (or niorr than o5 nidi ion \'cars. The clcsesl known rtdati\('s of laanv of 
die f^alo (jTlaccoLis Mahigas) laxa arc pcnccontcni|)orancons lorni> fi-oni South \incrica (priinariK \i;^rntina) and India, dius 
docurncnlinj^ a prcvioiisl}' nfircco^-niz(Ml hi*^h lc\("l of cosmopolitanism amon<^ (^ondwanan vciichralcs near llu' taul of the 
Cr(UaccoMs. The faniily-levcl laxa Miat arc shaicd anionic Madai^ascar. Sondi \mcri<-a. and die hidian sul)conlnicnl ai'c not 
known from penccont<'inpoiancous hori/ons in mainland Africa, hut It cannol \ct h<* conrid(aitl\ determined if diis is du<' lo 
dillerenlial cxliiution. p(jor sampling, line ahstaice (i.e.. the Ia\a were ne\ er |trc,-^en[ (jn AfVica). nv some (■orn]>inalion thereof. 
Nonetladess, (an-naitly availahlc geologic and j)alconlologic data aiv most consistent with the Arri<-a-rir^l niudtd, snggcsliiig 
tlial Ah'ica was I he first (tftjir major (iondwa nan lamhnasscs to he hd ly isolated priftr lo I he Al!»ian/('enomanian l)oun(hir\, and 
that its Itarestrial vcrtchiate launas hceame piogri^ssivelv more provincial <lining tlm (actaccous. wliih^ those on other 
(iondwaitaii 1andmass(\s reinalnod rclati\ely cosmop(tlitan until the latta- stages of lh(^ l.ate Cretatuious. 
t\('y ivonl.s: liiogeogi-aph\ , Cretaceous. Madagascar, Sonlli America, \erlel)rato^. 


Ld proy(M'to (U- la cnenca (U- Maluijanga. ini<'iado en ]WA y emtrado en los csliahts d<d Ca-ctacic(j supcrioi- cii (d noK teste de 
Madagascar, ha resnllado en el des(aihiimiento dc algiinos de los espcefmenes in;ls completos, iTicjor j^resciA ados y mas 
significatlxos d<- animales \<'rlel)rados tlcl Cretacici) lai'di'o del henhsfcrio sni \ (K- lieeho del miiiido. lailn^ los halla/gos mas 
imjjortantch Mai los vari(j> c>pccfmcnc.-% de crocoddifoirncs. dinosaurios no-auarcs \ maim'fcros; esto.s lialla/.gos licnen e] 
potcncial tU- adentrarsc en ])unIos cla\cs en la hi^toria hiogeogralu a y palcogcografica dc Condwana. Madagascar ha cstailo 
(fsicami-nte aishnla ile Ahiea po[- tmis dc l()0 millone 

s (\r anos \ dtd reslo de masas i 

Ic n: 

mpoi'lant<'s dc licria ptn' mas nc oo 
milloncs i\v anos. Los ]^ari(Miles c(MT-anos conotddos de muelio^ de los tavoncs malgaches del (a-(Macico larfh'ii s(tn formas 
penceont(Mnp(>r-aneas dc /\ni('riea del Sur (solkre todo de Ai'gentina) \ hi India. d(»enmen!ando asi' nn aho ni\el eosmopctlila 
j)re\ianuaitc desconocido (ailre ]o^ V(a1cl)rados d<" f^ondwana ctaca del final <lc] (aetacico. l.os la\on<!s al ni\(d dt- hnnilia 
comparlidos enlrc Madagas(\ir. \nierica d(d Sni- \ el >id)C(iiilinciite Indie no s(^ conoccii dc horizLiules ptaiccont<'mp(H-aiico^ de 
Afiica contintaitah piM-o !oda\ I'a no se piicde delerminar con eiate/a si esto se dche a cxtincion difcrenciada. escaso mneslreo. 
ausemda \(a<ladera fi.c.. los la\on<'s nunea cslnvicion pr(\senles en Airicaj. o inia ( leria r-omhinaiai'm )|(^ <-sos. No ohstante. los 
datos geo[(')gieos ) pah'ontoh')gii(}s acliialmentc [lisponihles son los mas consistiailcs con (d mi)dclo dc Afiica-primcro, (|ne 
siigiere (|iie \fiaca hie la ])rim(a-a d<' las masas itiipcMtanlcs dc lieria {]v Condwana ijiic cstu\f> aislada c(jmjilclameiitc antes d(d 
hmile (ltd Alhiano/dcnomaniano, v (jiie su lanna dc \'crttd>rados Ua^vslres se \"ol\ io ]>rogresi\ anitaite mas ]iri*\ in(dal duianic el 
Crelacico mienlras ([uc aqnellos en las rnasas t<'rrestres de (;()rii|\\ana iiermanecieion relati\ anicnic cosmopolitas ha>ta las 
fases linale.s did Ci"<'lacieo tanlat. 

We ihank the organi/ers lA the symposium and ihe editor's of tliis volume foi' ihc iii\ itatiou lo parllt i[)ate; om collahoralors 

a I the Uiil\cisity of Anlanauat I\o and llic Instil ule for the Ctaiser\ ation of Tropical Environments and die people ef iM-rivotia 

for logistical support; M. I lade 1 1 ami IT l{idg(d\' (oi- drawing l^gur-es TR and .~>l>. respeeli\ (d\. and h. IJeUi-NasIi lor c\e(mting 

and compiling all of the rfanaiiung figures; M. (^arrano, C. forstta". J. Ccorgi, J. (";roenke, \. Kiev, M. Loewen. T. Pira^gar, A. 

TuriKM-, and h. W ilnua- lor ad\'iee on fossil restorations; I., jacohs. I). Rowley, and i'.. Scot esc for dis(aission; P. Serraio and J. 

\\ ihlc lor insighthil i-cvievv of the manusciipt; and tlu^ Nati(tnal Science^ Foumlation and the Nalioual i a-ographic Societv h)r 
financial supjiort. 

~ Department of Anatomical Sciences, Stou\ Hi'ook riu\ (M-sit)-. St on) Biook, New\ sh.cdn 

^Dcpailmenl of Biomedical Sciences. 22<5 lr\ine Hall. Ohio I niversity, Athens, Ohio 4.">70l. L.S.A. 

' Paleontology Department, Sci(aice Museum of Minnesota, 120 \\T..t Kellogg liiMile\ard. Si. PauL Minnesola ;')SI02, L.S.A. 
Hltah Mnsmim of iNalmal Ilishtry and Dc|iarlm(ai1 [)f Geology and (^eo]>liysics, Lanvcrsity of Utah, 1390 East Presidents 
Circle, Salt Lake City, Ltah Mil l2-00.S(t, U.S.A. 

''EvcKn T. Stone Lui\(asit\ (a)ll<''!;e, Roosc\ell Uni\crsit\. (Jueaiio. Illinois (j0()05. L.S.A. 

■ Dej)artment of (ycohig), Maealcslcr (College. 1600 Ciand A\t luu'. St. Paul. Miimi'sota o.SIO.'i, L.S.A. 

York 11791-B(KJL L.S.A. 


\\\. Missoiiii BoT. (;\i!i). 93: 178-208. Plismmikdon 23 Aucist 2006. 

Volume 93, Number 2 

Krause et al. 

Late Cretaceous Terrestrial Vertebrates 


The first questiDii tliat logically might occur lo braLeis are the focub of this re[H>il because th(^y are 

n^adfMs of this conlril)iihon is "Why is Madagascar lied to land (some presumably itiore tlum others) and 

relevaiil to a consideralioii of Latin American bio- avc thus the most appropriate vertebrate animals (i.(\, 

geography?'' The answer is not intuitively obvious rehitive to, for exam[)le- fishes or birds) for examining 

Ii(H-ausc over 7500 km separate the two landtnasses biogeographic hypotheses involving subaerial land- 

todav and Madagascar's extant biota is highly endemic masses. We specifically h>cus on crocodyliforms, non- 

and inibalanced. However, in the context of a mobilist avian dinosaurs, and maiTiinals for the simple reason 

paraihgm of Earth history, the question has different that their representation in the (^ond\vanan terrestrial 

degrees of relevance depending upon the geologic fossil record is better than for most other terrestrial 

tim(,^ interval under consideration. We will assert in vertebrate clades an(b as a result, their phylogenetic 

this paper that near the end of the Late Cretaceous tlie relationsliips are more highly resolved. This repoil is 

island-continent of Madagascar hosted a terrestrial 
vert(d)rate fauna that was strikingly similar in 


not a comprehensive analysis of Gondwanan bio- 
ge()gra[)ln. Rather, it is an attempt to compan^ and 
tavonomic composition to that of South America. This evaluate the currently available data provided by 
high degree cjf similarity is unexpected in the context terrestrial vertebrate fossils from major southern 
)f most recent paleogeographic reconstructions, which landmasses, particularly Madagascar and South 
depict die southern superconlluent Condwana as AmcMica, in the context of n-cent paleogeographic 

r(M (Mist ructions of Condwana. We also stji\e to 
landmasses by this time. Specifically, Madagascar, identify and draw attention to sampling problems tliat 
althondi still connected to the Indian sulx-onlinent, js limit our al)ility to address particular biogeographic 

% J 

usually illustrated as having been physically isolated (jueslions. 

from all other Gondwanan landmasses since a|)[)ro.\- 

inuit<'ly 120 million years ago (Ma). This |)resents ^ri-;i{[u-:sTRlAt, VKHTEBtiAIT.S FI{(X\l I IIK Latkst Ct^ETVCEOes 

having long been fragmctited into its constituent 

a biogeograj)hic conundrum, as noted l)y Hay cl al. 

The configuration of Condwana changed dramati- 
cadv dining the I_.ate Jurassic and Cretaceous as it 


The sample of latf^st Cretaceous (Maastricht ian) 
vertebrates from Madagascar is llie most diverse and 
broke apart into isolaletl landmasses. The disj)ersion arguably the most significant in terms of comphMeness 
of these landmasses undoubtedly had profound 
consef[U(Mices for the geographic distribution and assettihlages 
subsc{[uent evolutionary lraj(x:tories of the resident [)articularly striking considtM^ing the small size of 

and preservation of specimens among Gondwanan 

outside of South America. This is 

teirestrial vertebrate faunas. Reconstructions of ih^ 
Mesozoic fragmentation of Condwana, hoAvever. an 

Madagascar; indeed, mainland Alrica. the largest o( 
the Gondwanan landmasses, is o\er 50 times larger in 

based almost exclusively on geoj)]iysical and strati- area and yet it^ pi^necontemporaneous vertebrate 

graphic evidence and remain poorly tested paleonto- fainia is much more poorly known, 
logically. Recent discoveries of fossil vertebrates on The vast majority of specimens known from the Lat(^ 

southern landmasses, particularly from the Late Cretaceous of Madcigasear have been discovered as 

Cictaccous of Madagascar (cL Krause et ah, I99*J; a residt of the Mahajanga Basin Project (MRP), 

Krause, 2003b), complement those known from South conducted jointly by Stony Brook University and the 

America and elsewhere and have profound implica- University of Antananarivo. The MBP w^as initiated in 

tions for testing hypotheses concerning the timing and 1993 and has included eight expeditions, the most 

sequence of Gondwanan breakup. Purportedly iso- recent in 2005. It is focused on the vertebrate 

lated in the Indian Ocean for o\'er 85 million years, pahninlology and geology of Upper Cretaceous strata 
Madagascar is of unique biogeographic importance; it 

in the Mahajanga Basin of northw^estern Madagascar 

occupied a central geographic position within Gond- (Fig. 1). Most of the fossil vertebrate specimens have 

wana and was among the first (western margin) and becji recovered from a small study area (measurin 

last ((^astern margin) majitr landmasses to be involved approximattdy 20 sq. km) iit^ar the \ illage ol Berivotra 

in fragtnentation of the supercontinent. and from one thin stratigraphic interval (measuring 

The objecti\e here is to [iro\ ide an overview of the some 12 m thick). Existing stratigraphic data indicate 

that this interval, the An(^mbalemba Member of the 

from the latest Cretaceous stage (Maastrichtian) of Maevarano Formation, is of Maastrichtian (latest 

Madagascar and to com[)are it with i)enecontempora- Cretaceous) age; however, we cannot discount the 

neons and earlier assemblages from South America possibility that lower rea<'hes of the member might bi; 

landmasses in an attempt to Campanlan (Rogers et al., 2000). TUg Anembalemba 

terrestrial vertebrate assemblage recently recovered 

1 otl 

and oin*^' 



elucidate biogeographic patterns. Terrestrial verte- 

Member is of fluvial orii^in and ai-cuiuulated in a semi- 


Annals of the 

Missouri Botanical Garden 

46° E 

47° E 

15° S 



j—M .- 

I '" 

Betsiboka limestone 


Berivotra Formation 


Maevarano Formation 


Marovoay beds 


Ankazomihaboka beds 








40 Km 



iiic L 1 \ir licrivotia Stiidv Vi^^a in llir Mjdajang;! Basin lA' nortliwrshan Mada^^ast ar and llir tuilnop aiva t^f Tppt |- 

Crclaccous am! MaKoiaan' ^liata in llir hasin. Oiirslion tnaiks intlicaU^ unciNlainU ( tHK-rrniriii a^^' rsliinalions. 

arid srlling C'!uir;ul<'i-ize(l l)\ rc|)clili\ r Hood e\('ii[s onh kiKtwii occiirrctices frniii Madagasfvir. fossil oi 
tliat li'iuiiered fi 


^ ..lU'-^raiiU'd drhtis llows. Tlios(' d(^tti'i 

Recent (e.g., gotidwanatluM-ps (Kraiise et al., IWThj 
Hows ill luin served to etiloml) and |hvs(M'\(' iiiassi\(' and iiiaisiipials (Krause. 2001) aiiioiiii mammals), and 
(|uaiililies of \erh'l)iale .-.Lelelal nialetial (lu)«iers el some rej)iesent the first l.ate Cretae(M)iis recoids from 

large jioilions of (w)iidwana (e.g.. lizards, birds, 

Sliidv ol diese \'(M-t(^l)rate fossils and the sediments 

ah. 2()()(): Rogers. 2005). 

Our ongoing edorls have drainalieally increased the 
])rev!onslv known (pic-lOO']) species diversity of i.ate 

(;retae<'nns \-ertel)rates from the island (eh Krause el that encas(^ ihem pro\ ides important information on 

ah. lOOia. 1990; Ki-ause. 200."5I>). d1ie lamia is now the anatontx. paleol)iolog\ . eeoloirv. and nhx loiicnetic 

known to include fishes, frogs, Imlle.s, li/ards, snakes, relationships of se\eral verlehrate higher ta\a and has 

crocodjiilorms, non-a\ ian dinosaurs, hirds, and resulted in im|)ortanl insights into, among othi^r 

numnnals. lVlan\ n(n\ genera and species have heen topics, the origin and eark exohit ion of hiiiU (For>ter 

discovered and many of the higher la\a rc[*resented el ah, 1996, 199!!. 2()0:5: Foisler iX O'Connoi". 2000; 

are the (irsl docum(aikM] occmreuces foi" die pre~Lale Chiusamy & El/anowski, 2001 ); the Conduanan 

di\ei-si Heat ion and d I si ri hut ion of croc()d\ I i forms 
(Bucklev el ah. 1997. 2000; Rucklev cK' liroehn. 

Pleistocene of Madagascar (e.g., frogs (Asher tK' 
Krause, I99[!), li/ards (Krause el ah. 2()():5a), hirds 

(Forsl.a-el ah, 1 990), mammals (Krause el ah. 199 Ij). 1999; Hasmnsson. 2002; Rasmnsson .K" Ihickley, 
Fintheiinore. some of the higher taxa re])resent the 2001; Turner, 2001a, b), samlschian 


Volume 93, Number 2 

Krause et al. 

Late Cretaceous Terrestrial Vertebrates 


Table 1. CioroiMiCnnn <^rnrn\ froni llie Anenibal('inl)a laii^^ing (Voiii small atul gracilf t(j large and pcMiderous, 
Memhrr oT llic Mae\-afaM<) Fornialioii. Ijiper Ci"eta('tH)us there is a hi'oad range in sknll shape, from robust and 
(Maastriclitian). Maliajanga Hasiii. Madagascar. broad lo long and slender to short and l)lnnt. 

= Mahaj(ing<isiichus inslgnis (Fig. 2), originally de- 

scribed on lli(^ basis of a nearly complete skeleton 
lacking only the skulk is the first crocodylifonn genus 


Siinusuclius Pmrklcw Rrocliu, Krause & Pol 

Genus indel. 

Trcnifflorhanipsd Riiflelaiit & Taquet 
V1(Masiieliia incertac scdis 


'ininpcsiicnus i i lee 

hfis Pii 

Mdhtijdiigdsuchiis Buckley & Rroehu 
Genus indel. A 
Genus in^^lel. B 

and species from (he bate Cactaceous of Madagascar 
to be natued on the basis of MliV discoveries (Buckley 
& I^rochu, 1999). Since publication on this specimeji, 
two nearly complete skulls have been discovered 
(Buckley & Brochu, 2001). Mahajangasuchus was 
a large carnivore, measuring almost 4 m in length, and 
is disliuclive among crocodylilorms in exhibiting an 
extremely broad and flat, hippopolamus-like snout 

1 (1 


and deep lower jaw. 

SiwnsucJiiis clarki (Fig. 3) is a new. bizarre, pug- 
n(jsed species represented by a complete skull anrl 
(Sampson et ak, 1998, 2001; Curry Rogers & Forster, ailiculaled anterior half of a poslcraiual skeleton that 

2001, 200 I; Curr) liogcrs, 2002, 2005; Carrano et ab, were pndiimuarily described by Buckley et a 

2002. 2001; (TCounor <!v Claesseus, 2005; O^Counor, The blunt, shovel-like snout, deep cranium, poster- 
in press), and mammaU (Krause et ab, 1997b: Krause, oveiil rally posilioncnl occipital condyle, underslung 

lower jaw, and areas for extensive neck musculature 
are suggeslixc of burrowing ada|)tations, whereas the 

ic origitis of the highl)' 

2001 ); the biogeograt)hi 

endemic extant Malagasy vertebrate fauna (Krause 

et ak. 1997a, 1999; Krause, 2003b); and the anteriorly pnsilioiuMl jaw joint and clove-shaped teeth 

stratigraphy, sedimentology, and g(UK*hrouology of may rcflcci ada|)lati()ns for herbivory (Fig. 3). 
Upper Cretaceous rocks in the Mahajanga Basin A new species, Araripesuchns sp. indet., is beuig 

(Kraus<^ & llarlman, 1996; Rogers et ak, 2000. 2001; described by A. Turner (in press). It is known from 

Casey et ab, 200:5; Rogers, 2005). Perhaps most skidls and sk(;]etons of at least five individuals, all 

significantly, these discoveries have profound impb- recovered from a single locality, that reveal a small, 

cations for testing biogeographic hy|iotheses that, in graeile-limbed form (Fig. 4). Araripesuchus /.sy///^''(//- 

turn, address broader ([ucstions concerning the timing sangund represents the geologically youngest occur- 

and : 

secnience ol i roru 


Iwanaii fragmentation (Krause et reucc, yet mosi piimitive k 

nown niemoer ol the genus 


ak, 1997a. b. 1999; Sam[)son et ab, 1998; Krause, (Turner, 2004a, b; in press). 


Trenuitochdnipsa olAila Buffetaut & Taquet, named 

Madagascar that was described prior to inception o 


The record of Late Cretaceous terrestrial verte- on the basis of ihre*^ fragmentary dentaries, is die oidy 
brates from Condwana is spott) at best and therefore crocod) lih.rm sp(M-ies from die Late Cretaceous of 
diffieidt to anabv.e and interpret in a biogeographic 
context. Among th(^ vertebrate groups represented in the MBP (Bidfetaut & Taquet, 1979). A better- 
die Late Cretaceous of Madagascar, the best known in ])reserved (kailary, as weU as several skull and 
terms of their completeness and preservation and poslcrauial elemeiils. were recovered by MBP expedi- 
therefore the most precis(dy identified, are the tions (Hasnuisson c^ Rn.-kley, 2001). The new material 

crocodyliforms, uon-avian dinosaurs, and mammals. 

of r. oUila provides the opportunity for a better 


laxa are therefore the most relevant for uud(a-slaMding of pliylogenetie relationshii^s of trema- 


consideration of biogeograi)hic relationships. The 
following pi'ovides a britd" overview^ ol the taxonomic 
and anatomical diversitv of each of llu!se taxa. 


tochampsids; Rasnuisson (2002) determined that 
tixanalochampsids are mono] di) let ic, but that the 
genus Tn'nt(}f(K-h(iinps(i is paraphyletic. Although still 
poorly known, it is clear diat T. ohliUi, like 
\1<iha/(tngasiichus, was a massive animal and likely 
one of the to|) f^HMlalors of ils time. 
At least seven s[>ecies of crocodyliforms, all In addition to these named crocodylifonn taxa, 

metasuchians, arc prescnl in the Maevarano Forma- there are at least Mnee as yet unnamed species 
tion (Table 1). This diversity is extraordinai7, aufi it is recovered from tlu^ Maevarano Formation. One is 
therefore not surprising thai a range of adaptations reiiresenlcd by several skull elements preliminarily 
suggestive of habitat spcciali/alion Is evident. In identified as peirosaui-id. The second is a medunn- 
addilion to (^xtreme diHerences in body size and form, si/eJ (i.e., smaller than Maiuijangasachus insignis and 


Annals of the 

Missouri Botanical Garden 

Figiiiv 2. Mdliajdngasurhus i/isignis Bticklt-) cK llroclui. a lar^c, l.toad-iiioullu^l inrlasi]i'lii;iii (■n.((Hl\ lifnMii from \\ic l.aU 
Crt'lacoous of Mad.igiiscar. Skull iti IrCl lat(^ra] \\r\\ and rcstoralion of du' skull and sktdftou in \ri\ lalrral \ i.-w. 

Trcmutoiluimpsa uUild.hui hwy^cv {\vdn AninjH'surhus TcUmcL 197^); Sues, 19111); Fig. S). ()ti(^ of \\\v mosi 

sp. in(l<M.). slen(l('i--sn()iite(l iiH'tasiudiiati, irjjivsciilcd spcctacidar fossil (liscovci-ics of (lie MBI^ lo date is an 

hy a ]Ku1ial skidL a coinplcle lower jaw, and e\(juisitely preserved and \irtnall_\ e(nnplete skidl aiifl 

considerable |)osleranial iiiahaial (Buekh^y et al.. lower jaws of M. a f opus, diseo\ered in J 996 

2003). The third is poorly ktiown, represented only by (Sai]ii)son el al., 1998). Tlie short and deep skull 

isolated ebanenis, primarily parlial skull luul jaw hears fused 



)ones wnii a 


arge nilei lor 


M.).\-\\ I A.\ DIXOSALIiS 

Dinosani- malerial is abundant in the Mi 


))n(HUiiatie oIkuiiIxt, and a midline jirojeetioii or 
"horn'' positioned above the e\es, with a nolal)h' 
paru^al emineuee eaj)ping the skidl rotjf posleriorU . 
(^onij)lementiu<i; ihis specimen are seveicd oilier, more 
(ragmetitary, and less \v(dl-pieser\(Ml skulls diseov- 

Formation. but lo date is limited lo the Sauriselua. At rrnl recently, in addition lo three partial skelclon., 

leasl [our non-avian s[)ecies ha\f' been diseo\ered: 
Iwo lhero[)ods and Uvo sauropods (d able 2). 

one of thetn ]-e|)reseiUing a ju\enih; indi\ iduah ihus, 
virlually all bones ol lh(^ sk(deton are now represented 

Tlu^ best represented of ihe Iwo theropods is (he lor ibis animal (the prlniar) exce])li(»ns beinii pails of 
mid-sized (approximately 6.2 m in length) ab(disaurid die pelvis and the distal porlions of die forelimbsj. 

hi lo be Th(^se specitTiens confirm referral o^ Mdjungalliolus to 



ijniigdUioLus at opus, pre\'iousiv ifioug; 

Iv ll 

\u ( 


a pachyee])lialosaurid (■•doin(-h<\ule(r ornillnschian ihe Al)elisanridae and are descrlbet 

dinosaur) baset! on bai^inentary skull malerial (Sues & a tTionogra])li-h'ngth sludy (Sanii>sou & Krau>(% in 

Volume 93, Number 2 

Krause et al. 

Late Cretaceous Terrestrial Vertebrates 


Simosuchus clarki 


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Fi-un- 3. Simosuchus clarki Buckley, Bn.clm, Krause & I'ol, a sniall- l<> mid-sized nuMasuchia.i erofodyliform from die 
LaU^ Cretaeeous of Mada|2;asear. Skull in left laU-ral view and re^lonilioii of die skull and skeleton in left lateral view. 

ss). Numerous l)oiies in the iMaevarano assemhlage et al. (2001) and Carrauo et al (2002), win. eoncduded 

lliat tliis Malagasy taxon should be inrduded within 
tlie sinalM)()died abelisauroid claclc Noasauritlae, 

exhibit tooth marks (some of vvhicli even i)reserve 

denticle drag marks) lliat ran be attributed only to 

Mdjangalholas, thus attesting lu its eaniivorous 

habits. Interestingly, many of the bones are those ot 

Majiingatholiis itself, thereby providing the first well- poraneoi 

documented evidenre for cannibalism among dino- (previously known only from Argentina) therefore 

previously known only bom Argentina. The [)lat:eineiit 
of Masiakasdurus — together with the peneeontem- 

s Inflian form lAicvisachus — into Noasauridae 


saurs (Kogers et ah, 20(K^). 


reatU expanded llie geogra|)hic range of this clade to 

Masiakasaurus kfiopflcrL measuring approximately encompass much of Condwana. This finding d(Mnon- 
1.8 m long, was a much smaller a!id more gracile slrates dial, at least in a number of ecosystems, 
jtredator than Mujiingallwlus afopus (FMg. 6). ll is noasaurid abelisauroids were small-bodied counter- 
represented by isolated bones of both the skull and parts to their larger-bixhcd cousins, the abelisaurids, 
postcranial skeleton and is thus less comidetely in a maimer parallel lo small-bodied maniraptoran 
kimwn. Masiakasiiunis is remarkabh^ however, in coebn-osaurs (e.g.. troodontids, oviraptorosaiu-s, dro- 
having an anterlcn- dentition that consists of pro- maeosaurids) and large-boded tyrannosaindds in many 
cumbent, spearing tecdh, a unique condition among Late Cretaceous Laurasian ecosystems. Recent fu l(b 
DirK)sauria. il/a^m/.7Ma;au.s vvastles(rii)tHl by Sampson work in 2003 and 200r> has produced additional 


Annals of the 

Missouri Botanical Garden 

Fio;ti!v 4. Auiriprsurhus sp. iiulcL, a small. 'i,ra(al(-liiiilnM| iiiclasuclilaii cnxodMimr 

Maclatias<-ar. Skull in left lateral \ic\\ and i-csUn-alion '»(" [lir skii 

lilntni [\\m\ tlu' i.alc CiTtacrniis dT 
and >k(d(^to(i in left lalrral \ i(n\-. 

skclelal remains o\ MasUikasdunis. iiicluillM«! several 


key, previously iiMi-e])|-esente(! cranial and jxtstcrarual 
elements tlial will >imnfiean[K increase knowlediz-e of 

noasanrid anatomy (Cairano el al.. 2()()4, in (n-cp.). 

Tahle 2 

Non-a\ ian (liiu)sai]i- f^cncia from llie Aiic 



irnnxT () 

r ii 

H- Ma<-\ aiario Fornialinn. U[)pci 

CrctacfOLis (Maaslrichlian), Maliajan^a Ha^iii. _Mada<i;ascar, 


II )()( la 




.Majtingdlhulus Sues tK Ta(jiicl 



MdsiakdSfjHrus Sain[)S()n. (lairano iX Foi-sli i 


rn * 



t:irnu^ Jnil<*l. (Malagas) Taxon W of (anrA Itoi^c^rs. 


I jllio.^trolia inccritic sedls 

Riipciosdunis Cni"i\ Iu)U(M"s tS.^ r'orsler 


' I < 


sanropods were amon<^ the In'st 

fossils d<^scril)ed Froni Mackitrasear and aie ahmidanl 
componenls of ihe Lale Cretaceons fauna. At leas! two 
s[)ecies of lillioslrotian lilanosaurs are [»resent In (lie 
(anna, antl al leasl one ])ossessed oslendernis (''skin 
hones'') ihat range in size from small ossicles to hony 
plales greater [ban 10 cm in diameter (Oeperet. 1 89(); 
Dodson el a].. 199a). 

R(ipeli)Siiiiriis Irausel is known from aj)pnixima[ely 
90% of its skelelon, including several \\ell-])veser\ cd 
associated specimens re|)iesentinu' a range of milnge- 

nellc stages (Cnrry Rogers S^ Forster, 2001, 200 1; 
(an-ry Rogers, 2005; Fig. 7). Rapelusaurus is (»arlic- 

ularly signilieani I)ecanse it pres(u-ves cj-anial and 

post cranial data ke\ to elucidating pli)]og(audic 
relalu)nslnps among one of the most tem])orallv and 
ge(tgra[)liically widespread of dinosaurian groups. 
Rdjx'losatirus has already ])i-o\id(Ml the first cranial 
dala in su])porl ol Titanosam'ifttrnH^s mono[)h}ly and 

on o 

r I 


ower-n'\ e 


has helped lo increase rcsoluti 

lilauosauiian r(dalionshi[)s (Curry Rogers & Forster, 

2001; Cnrr) Rogers, 2005). 

Volume 93, Number 2 

Krause et al. 

Late Cretaceous Terrestrial Vertebrates 


Majungatholus atop us 

.' * 

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Figure 5. M ajungalholas aiopas Sues & TaqueU a inid-si/ed llieropod (Jinosaur from the Late Cretaceous of Madagascar. 
Skull ill left lateral view and restoration of die skull and ski^lelon in left lateral vi(nv. 

"Malagasy Taxon B" (Table 2) is the second agnostic: Malagasy Taxon B exhibits a square coracoid 
titanosaur species from Madagascar. AUhongh repre- with ])road scapular facet, whereas Rapetosaums Inas 

a rounded coracoid Avith narrow scapular arliculalion. 
Curry Rogers (2005) recently conrlucted a phyloge- 

senled by only several isolated caudal vertebrae, 
a series of articulated distal caudal s, and an isolated 

coracoid (Curry Rogers, 2002. 2005), Taxon B can be netic analysis and concluded thai Malagasy Taxon B 

easily distingtushed from Rapctosaurus. Tlie caudal and Rapetosaurus are distant ridatives withiji Titano- 

centra of Malagasy Taxon B are distinctively dorso- sauriformes (Curry Rogers, 2005). Even more signif- 

ventrally compressed and subrectangular in transverse icantly, the compressed caudal vertebrae and io^v 

section. In contrast, Rapclosaurus caudal centra have neurcil spines of Malagasy Taxon B indicate dial it is 

subequal height atid width dimensions resulting in a member of Saltasaurinae (sensu Wilson & Up- 

a rou 

nd transverse section, Coracoids are also di- church, ! 


witn Close 

lose affinities to llie South 


Annals of the 

Missouri Botanical Garden 

}i<iuic 6. 

MiiS!(,h!s<tnrus hnopjlni Sani[>son. Carnitu* iK l-orstrr. a small llinopod diiiosaui- fiotii iIjc I.aU- Crctacroiis of 
Madagasrai". Skull In Icfl lalcral vi<'\v and rv^loratioii of tlic skull and skcdclnn in h^Cl laloral view. 

Aiiiericaii sallasauriiic genera Sdhasdnrus^ ^^euqurn- l^asacL v. hi Kocni-^ualtL Saluii cK Crine, a sudanuM- 
sduras, and Rnrasaiinis. jcid c.„n(l\vanalIaMr (Krause et al.. 19971)1 Siidanier- 


s are nm([U(' among 


irso/oic uuunniais \i\ 



Tde Late Crelaeeous tnaninialian fauna of Mada- 
gascar is sLill poorl) understood. Il is represented Nv 
five, or perhaps si>:, taxa, eaeli known from nolliin^ 

possessing hy|>sodont clieek-leelli separated fr(HM 
gliriform incisors l»y a prononneed diaslenia. Jusl as 
(or noasanrid (lieropods (see al)o\c), the diseover> of 

sndamtMicids in Madaij;ascar and die Indian 

eonlinent considerahl 

\ e\ 



tended die geographic range 

more than a fragmenlary tooth or two (Krause et ah, of the elath- (previously kuovvn onlv from \ 


1991 1997h; Krause & Grine, 1990; Krause, 2()()U an(! pn)vl(hd evidence for a previously unknown high 

2002; Tahle ,'5). One stili-uJidescrihed laxon, liovvev(M\ 

is re[)resented hy a nearl\ cornplcle, wtdl-prescrvcMJ, 
and articulated sktdelon (Krause, 20{):5a). Interesliu'i:- 

ly, none of ihe knctwn taxa can he considered to !)e 
])otenlial ancestors of the ishuuTs hi^ldy endcniic 
extant luammalian fauna, all of vvhicdi ai'e [daeeulals. ancl eonsiderahh 
Two fragiuenlarv matTimalian lecMJi were assigniMl to 

degree of cosmopolitanism that enconi|)asscd hoth 
western and <'astcrn Couchvana (see below). 

At least on(^ other tootli may also be assi^iiicd to 

Condwanadieria (lisltnl as Mannnalia incerlar scdis 
Getujs indct. A in Table 3), although il is niu(di larg<M- 

ower crounec 

I llu 

ni those assigned 

to Laraitijy (Krause, 2000). Still less hiuh-erowne* 


a new genus and species, Laiamfy nilolaka Kraus<', another isolated looth that exhibits a .-omplex occlusal 

Volume 93, Number 2 

Krause et al. 

Late Cretaceous Terrestrial Vertebrates 



■e i . 

Rapefosnurus knmsri Curry Kogors t< I'\h-sI(m\ ;i liUiiiosaiirid saiiri)|KKl dinosaur fVotn tlic Lair Cielaceous of 
Marla^ascar. Suhadull skull in Icfl lalcral view and rrsl(irali»tn of du- skull and sk(dcl()ti in UAi lateral view. 

niorpli(d()gy (W-sliapod ridge with two infiiiKlilnda l)asiHl on cuneiiL liifornuilioii, it could equally well 
separating eacdi of llie ihn^'e lim!)s o( the W) on an 

jeiong to a previously unrecognized liigher taxon of 


obliqnely-oriented surface. This speeiineu coidd Mesozoic nianunals. 
conceivably also pertain to (^ondw 




Tal)le 3. Mammalia II genera f|-()tti the An('inl)alemha 

yVnolher isohiled loolh, a trihosphenlc lower molar, 
w^as legarded liy Krause (200]) as ihal of a marsupial 

Member of die Maevarano FernuUlnn, Upper Crela<;eous and tlH-refore as polenlially the earHesL evidence of 

(Maaslrielitian), Mahajanga Rasin, Madagascar. 



Genus indet. 

Ci-nus indel. 






Lavaiiifv Krause, Prasad, von Koenigswald, Salini l^' 
Mammalia incerUie sedi.'i 
(i-enus indet. A 
Genus indet. 15 

marsupials in the Southern Hemisphere. Tliis identi- 
fication was eoidnnied by Case and Krause (2002), 
but lias sijice been disputed by Averianov et al. 
(20()-*V); Case (in prep.) is nearing comjiletion of a more 
detailed analysis that supports the marsupial aflinitles 
of the taxon i-epresent(Ml by this specimen. 

Another isolated speeinK^i is a molar fiagment 
exhibiting cusp- in-line morpholog)^ characteristic of 
mullituberculates, a (dade that is well represented and 
extrenudy diverse in peneconlemporaneons, as well as 
earlier and hiter, horizons in Laurasia (Krause & Grine. 
1996). Multiluberculates are poorl\- known from the 
Mesozoic of the Soudiern IIemis[>here, prexious!) found 


Annals of the 

Missouri Botanical Garden 

bla^ics (>( Mada^'ascar and Soulli Ainciica. However. 


tile laxoiiomir siniilarilies IxMween [\\r asseitihlages 

al ll 

le eiH 

f tl 


only in llie V.i\\\\ CEvlaeeous of Moroeeo (Si^()<i,tu'au- 
Puisriell, 1991; tlaliii v^S. llalin, 2(){);^) and |K.ssil.l_\ llie 

Lale Cretaceous (Campaiiiari or earl) Alaaslrieliliati) of (rum lln^se two laiidnia^se.s 

Argeiiliiia (Kielan-Jawonnvska et ul., 2001). Cretaceous make it e]ear lliat physical and l>iolic 

Finally, one recently discovered laxon (listed as connections widi olluM" landniasses were al>o ifi\ ol\ (xl 

Mammalia inccrlac scdis (^enns ind(M. I> in Tabic '.]) is and tnnst he considered. An overview of j)(^neconte]i]- 

represented h\ a virtually coni|»I<-le, articnlalcd. s[il>- poratieoiis terrestrial Taitnas from polcntially con- 
adiilt sk(delon (Kranse, 2{)(na). This skeleton, still in nect-^! lan(hnasses— namelv Antarctica. Africa, and 
llu^ process ol hein^ prepared and studied, represents the Indian snl)cotilinent — is therefore warrant*^!. 

the largest and most comphMf^ spe<'inien of a mammal 
yet known fr<Mn the Mesozoic of Condwana. It e\hil)its 

(e.g.. septomaxilia with 



ng mosaic oi [)rinHti\(' 


Auslialia and southern Europe also contained (iond- 
wanan-aspecl faunas duiing [he T.ale Cretaceous, l)ut 
tluM-e Is no iiidependent evidtaice inclicaiing that 
proitiinent septomaxillary canal, ejiipubic hone) and either was J/m-//j- conui-cted to Madagascar or South 
(haived (e.g.. sp(H*ializ(Ml (hattition with proiuiuenl America durnig ihis interval; as such, and owing lo 

space c-onsid<Matioirs, llicir faunas are not considered 

nuunmalian ph\logenv. It is also sale to conchule. 
even at tins preliuihiary stage, lliat this animal cannot 
1)1" ''shoehorned" into any (anrenllv recoiiiii/ed liiulicr 
laxon of mauunals; it i"ep resents a majof new 
nontherian clade. Tlie relati\(' conn)leteness of this 
(Wti-aordina!) speciuuai promises to elui-idate the 
analoun. functional 

morphology, and plnlog(M]et i( 

position ol tlie (dade it represents. 

'ri:iun:sT!n \i. \KtMi:tii{ \ti^s ki^om tiik 

ANKAZOMIM \l!()ts\ ^WDsiOM^S 

Teri-cstrial \'ertel)rate fossils have also been re- 
covered Ir-oui the Aukazomihahoka sandslones, a unit 

thai is purportedly interheddcd with, and diTinlltdy 
o\'(M-|ies, hasalls of Coniacian age (Re^sairie, 1072; 
Storey el ah. J 993, 1997). A prelimniaiy rej>orl 

(Curry. 1997) inilicates the preseue<^ of at least tluce 

crocod) lifonTi taxa and two to iIuxh' taxa of notiavlan 

dinosaurs, including sanropctds iuid tliei-o])ods; no 
ruafunials were lound. Suhs(M|ueut collections liave 
hetai made and a more extensive aualvsis of [lie 
ass(Miihlage from diis unit is under wav fCurrv [{oilers 
et al., in [>rc[).). The taxa d(M-i\ed from the 
Aukazomihahoka sandstones are not considered Ikuc 


)ei.;ause o 

f tl 

u^ tentative.' nature 


f ll 

le curieni 

)ecanse tlu' age <>( the rock luiit 

identifications and I 
has not been ascei'tained. although, eonserx ativelv. it 
ran he conslrained to liave been as earlv as Coniacian 
and as late as Maastri(ditian. 

C\^u^\^lA^/MAASt■|ael^l■r\^ CiioconM.ii-oiiM.s, 

N(),\-AVIA,N DtNOSAI IIS. AM) M AM \] \l> I'l^dM 

OntKK G()\ti\\\,\AN hAiNUM \ssi:s 

The pi'imar) purpose of this section is lo couipare 


diastenuK well-developed hu[U(aal trochlea, r(Hlue(Ml 
fihular-calcaueal eonlaci) features. There is no (louht | 
that this specinuai will introduce a snhstanlial aiuounl 
of charael(M- conflict into pre\ ious topologies of ^f [ 

The lauual lists in Tables 4—6 proxide an overview 

le geuia'ic (H\ersitv of crocncb liloiius. non-a\ian 
dinosaui-s. and mammals known from (he ('ampaniaii 
and Maastrichlian stages of South America. Africa, 
Antai-clica, and the Indian subcontinenf. The Campa- 
nian and Maasirichtian. the last two stages of the Late 
Cretaceous, i-e|)resf^nt a broader lime slice (approxi- 



(kS mi 

ion years) than is likely repres<Mited 

by the Anetnbalemba Metiilx^r of the M; 


Formal it)n in Madagascar. Nonetheless, lln 

' uneven 

coui])aris(tn is neeessilat<Ml, al h^asl in part, because^ of 
the j)oor sam|)ling of |)enecontemp()rane()us (Jondwa- 
nan hoii/ons and because of the imprecise datiu"^ of 

1 O 

productixc strata; gixcn iht^se constraints, il is better 
to be loo itudusive rath(a- than Voo exclusi\(!. The 
faunal lists have Ixm-u extracted from mimerous 
sourc'cs lor crocod)l dorms (e.g., Gas|)arini v\ ah. 
1996: i^crtiin & Carvaiho. 1909: W ilson et ah, 2001; 
l^rasad ^X de Lapparenl de Hroin. 2002). but primarilv 
froiii \\ eishampel el al. (200 I) foi- non-a\ iaii dinosaurs 
and Kichui-Jaworowska el al. (2001) for mamtuals, 
with otiicr sources noted in table lu^adings. 

SOUTH \\u-;iue\ 

South Artuaiea has the larg(^st and tuosi di\ei-se 
sam[>h*s o( (iondwanau l.ale Cretaceous \ erlebrat(\s, 
many fi'om Cami)anian and Maasirichtian horizons. 
Indeed, tlieie are o\'(^r K) fami]v-le\(d taxa of 






/vmerica. more 



terrestrial xcM'tebrates know n fi- 

and Maasirichtian of South A 

double the number from any other (^ondwauan 

landmass. This is in large- part the result (>[ intense 

sami»ling over the pasi several decad(^s, much of il 

owing to the ellorts of Jose Honapartc of the iMus(n) 

Arj^cftilno de Cieucias Natnrales Paleonloloai.i (R 



nos Airesl and his students. 

It is not possible to (lelermiiu- which of the huuilv- 

the laU^sl Cretac(H>us terreslrial vertebrate assem- level laxa (;uri-entlv unknown bom clsewh(a'e were 

Volume 93, Number 2 

Krause et al. 

Late Cretaceous Terrestrial Vertebrates 


Table A. Crocodylifofin <^cn(M'a from Canipanian and 
aaslriclilian liorl/ons in Soiilli Amrrira, Africa. 
Anlanlica. and ilie Indian sMhrf>ntin(^Ml. LisI for SoiUli 


Atiicrica c-onipilod ])riniai"ily (nmi Casparini (1.996) and 
R.Ttini and Carvallio (1999), for Africa from Buffotaut (19H2) 
and Rt'DcIiu (1 997), and for llir Tntlian sul)('{)ntinoiil froru 
W ilson r[ al. (2001) and Prasad atid dc Laj)[)areiit de Ri't)in 

Soi ill Amkrica 







Uriiguaysuchiis [{usconi 

Crnodojilosuchus \\ tjodward 

Baurusiiclnis Vv'we 

Slrdliolosuchus Canipo,-,. Suai'oz. Riff & K<'Mnrr 

Pcirosditrus Pi'ice 

Lonmsiichns (^aspaiini, (diiafipo & Feiiiandiv, 

inae)), and mammals (Su(]amrilfidae) thai }ia\c ])ol'ii 
identified as ocoiirring in ihe Maastrichtian of 
Madagascar, all are known from the Campaniaii/ 
Maastrichtian of Sonlh America. This is suggeslive of 
close biogeographic lies aiuh indeed, a degree ol 
cosmopolitanism tliat was nnexpected before llie MliP 
(hscoveries and lliat. moreover, is difficult to explani 
in ihe context of most recent paleogeographic 

CrocodybfoiTus kiiown from Campauian and \bias- 
trichtian liorizons in South America are diverse, 
comj)rising at least 12 named genera, most of them 
metasuchians. In ad(htion to notosuchids, peirosanrids, 
and trematochampsids, ihe melasuchian family Baur- 
nsuchidae is represenltMl. Neosuchians and eusnchians, 

fuj- whicii definiti\e evidence has )el lo be found in the 
Pate Cretaceous of Madagascar, are also })resenl in 

South America. The non-avian dinosaur fauna from iIk* 
South American Campanian and Maastrichtian is 

Uheniha.sKchus Carvallio. Rihriro & dos Santos Avilhi donunated by sauristdiians. Among Theropoda, ab(di- 

sanroid ceratosaurians (in( hiding 1x)di abelisaurids and 
noasanrids) are the most (Hverse and, among tlie 
Sauropoda, lithosLrolians, including saltasaurines, dom- 
inate. Ornithiscldans are represented by spolty occur- 
rences of ankylosaurs, enonuthopods, and hadrosaurs. 
It is inlriguing that, in conlrast to the dominance of 


Ifasurhus Price 
Mclasiudiia incertae sedis 

Sphiigesaitrus Price 

Sulcusuchus Casparini iN. Spalletli 


Hyposaurus Owen ((lucsiionahly from Maasuivhtian) ornithistdiian herbivores in most Campanian terrestrial 

Laurasian-d(M'ived landmasses, or- 

ecosvslems on 




Di'thchochampsd (iaspariin <X linffetaut 




D} [(jsauiidae 

Sokotosuchus lialslead 


No i'c(.:ord 

IM)l,\^ .SliIicoNTlM■:^T 






Pdhaehshi Wilson. Malkani & Gingerich 

Melasiichia incertae sedis 

nidnschlans appear to l)c only tninor conip)onenls of 
Campanian ecosystems on most Condwanan land- 
[uasses, if they are pres<ait at all (Currie, 1996). 
Campanian and Maastrichtian mammals from South 
America iTKdude a diversity of archaic nontnbosphenic 

forms, including Austrotriconodontidae, Bondcsiidae, 
Rrandoniidae, Dnolestidae, Ferngliotheriidae, Mesnn- 
gnlalidae, Reigitheridae, and Sudamericidae. 01 diese, 
only the Sudamericidae is known to also occur in 
a{higascar (Krause et al., 1997b). In addition lo this 
diversity of nontribosplieini- taxa, lliere arc two species 
of fnidierians and (}iieslionabh* occui'rences of ^^j)e(Ho- 
m\id" and peradectid marsn[)ials. 

Coiius indet. 




I)} ro^auiidae 
Genus indel 

Not unexpectedly, consid^M'ing its ice-cover and 

harsh climate today, Antarctica has grndgingly 

yicldiul fossils of f.ale Crt;laceous terrestrial verU;- 
iiideed restricted to SonUi Arnei"ica and whic-h were brales. rhey liave b(nMi nn-overed from the Anlarctic 
more broadl) distributed in the Southern Hemispliere, Peninsula (Vega and James Ross Islands) and intdude 
simply because of the relative paucity of rHscoveries only specimens of dinosaurs (Hooker et al., 1991; 
on other Condwanan landmasses. However, it is Casparini et al., 1996; Rich el ab, 1999; Case et ab. 
significant to note tliat of the seven family-level ta\a 2()()0, 2003). This ap[)ears to be largely the result ol 
of crocodyliforms (Notosuchidae, Peirosauridae, Tre- "'bhjat and float" taphonomic scenarios, wlicn^ 
malochampsidae), non-avian dinosaurs (Abeiisanri- carcasses are washed out to sea and skeletal elements 
dae, Noasauridae, Sahasamadae (inchiding Sallasaur- are buried in, and rec-overed from, marine seditnents. 


Annals of the 

Missouri Botanical Garden 

f"i 1 

I'ahle ^. Nt>ii-a\ Jaii dindsaur genera frorn 

and Maa^tin-lilian I 

loii/ons in Soul 1 1 Arnrrica, Aliica, 

Wilson and I fpciuntli ^200^^) for Indin. and Sul)('ii)i(>la el al. 
(200 1) lor Afr'ica. (^)ii(^slion niaiks indlcah^ I^'nlat i\(' 

Sol [11 Ami Kiev 



Carnofaunis nona])ai'tr 
Alx'lisaur'idai^ ind(M. 



Nodsaiinis Hoiiaparlc iX Poucll 




Qiidnu'saunis Coria 






,s Povvell 

y( )\ irajilnsauiia iiidrt. 
Coeinrosaui'ia indt^l. 

r I ^ 

]{M'(i])oda mdrt. 



Sdllii.sdiiriis nonaparlr <S Powell 
Lilluthlroha uu-crldv scdis 

Acolosaurus Pttwell 

AnUirvlosanrus I luene 

IjtphildSdnnis 1 iiinic, 

yciK/ucnosaurus Pfnvrll 

Pclliginisdiinis Sal gad o 

RocdSdurifs Salgado t^" A/j)ili(an't; 

i jthosh'olia indct. 

Tilanosauria iiulet. 
Sain'oj)()da indel. 


Tll^ ri'opliora 

Ank\ lor^ainia 


?Nodi)r^ain-ida(' indcl. 

Aiik\ lo^anl■id;^e indt.-l. 
Oi nillio[)oda 

Tdl<'nk(tu<'}} Novas, (^anihiaso ^^ Arnhiosi 



I Indrosanrinac indol. 


irnhcosannnae uu 


luioinitliopoda indct. 






A I 





Ccnu^ indi'l. 

Avcdicropoda inccrlac sedis 

Bdluuidsaiirus Slioniei 

Tab I 

e o. 


Anlarclii-a, and die Indian suix-onlinenl. 1 .isis eonipiled 
{row \\ eisliaiiijK'l et al. (2001). wilh addilions fruni No\'as 
and Agtiolin (2001). N(i\as et al. (2004) (or Sondi Aineriea, A^■T\l{(:|■l(: \ 


Ti I anosa nil formes iiid4'! . 

Tlierojioda indct. 

Ank\ losaniia 

Nodosauridat' iiidel. 


Fladrosatiridae iiidcl, 

iM)l w Si r.eONTiM-AT 




hidosdurus llin'ne & Mallcy 
Indosiiclms lliicnc iK Mallc\' 

Rdjasdu/ns W ilson, S(M'eno, Sri\asli\a, lihatl, 

Khosla eK Salmi 
Gcnii> indct. A 
Geiuis indct. B 

LdCi i.sucIiiL\ lliieiic X Malic)' 
('cfalosaui'ia Iiidcl. 
?Car]io>auria iiidet. 

Conipsosnrhiis Hiii-nc lK Mallr\ 
{)i"nitlif>miniidae indcl. 
rheroj^oda indct. 

I .itliosti'otia 

Isisdiinis \\ ilson iK L'jKhui'cl] 
Jdinosdurns Ihiiit, l.oekley, Lneas <!^ Mcyci- 
Titanosauiia nidel. 
Sanropoda indct. 
\]\\ reopln)ia 


Ank^lu.sanndac nidcl. 

Slegosainidae indel. 

I Ins also may acroimt for iIk' hi(d< of discovery of 
riinall verlebrale laxa (e.g., li/ards, iLittlcs, crocod}!!- 
fornis, nianiiiials), allliongli (dimale may have also 
played an imj)(>rlaiit role. Intert^slingly, llie dinosaur 
fossils thai have l)eei] roeovei'od arc of laxa (e.g., 
Kuornilhopoda, I ladrosatiridae, Nodosaiiridac) thai 
are not repn^scntcd in iIk^ (iatnpaiiian/Maastrichtian 
of Africa, Madagascar, or the hidiaii stihconlinetil. 

Inst(^ad tliev are shared wilh penei-onteiiipoicmeous 
hoi'izons in South America. 


Africa is, l)y far, llic largest (ioii(Kvanaii landmass, 
roughly 70% larger than \]\c next largest. South 

Volume 93, Number 2 

Krause et al. 

Late Cretaceous Terrestrial Vertebrates 


Table 6. Mammalian genera from Campanian and 

America. Despite its vast superiorlly in size among the 
Maastriehtian liorizons in South America, Africa, five C/Ondwanan landmasses considered here, Africa's 

Antarctica, and ihe Indian subcontinent. Lists compiled diversity of Campaniair/Maastriclitian terrestrial ver- 

Ironi Ki(dan-Ja\voro\vska et al. (I 

), witli additions from 

tlana and Wilson (20{)H) and Khosla et ah (200d) for the 
Indian subcontinent. Question marks indicate questionable 
occurrences and quotation marks indicate paraphyletic taxa. 

Soi ru Ami-:kica 


Reigllherlnm Bona[)arte 




Austrotriamodon Bonaparte 
?Mull]lubereulata Incerlae sedis 

Genus indet. 

Archaic '\symnietrodontans 

Bondesius Bonaparte 
Stem Cladotheria 



Croehcrtherinni Bonaparte 
Leonardus Bonaparte 


enus m( 



Mcsungulatum Bonaparte & Soi'ia 

Brandon iidae 

Brdndoiiia Bonaparte 
?Cauun.igucdia Bonaparte 
Marsupial ia 


ruis ni(_ 


Genus indet. 

Family incerlae scdis 

Perutherium Crambast, Martinez, Matlaucr & flialcr 

Genus indet. 




GondwanalJieriuni Bonaparte 

Ferugliother'nwi Bonaparte 



o recor 




o recorr 


Indian Subcontinknt 



(jcnus indet. 

Family Incerlae sedis 

Deccanolestes Prasad & Salmj 
Sahnithcrium Rana & Wilson 
Infraclass incerlae sedis 




Genus indet 

tebrates is the second poorest, little better than that 
from Antarctica. This is pr(;suiriably due in large part 
to the virtual absence of suitable sedimentary 
depocenters of the right age and environment, but 
further exacerbated by limited exploration and a lack 
of definitive age control indepeirdcnt of the verte])rate 
fossils themselves. 

Of the seven identifief^l (amilies of crocodylilorms, 
non-avian dinosaurs, and mammals represented in 
agascar, only one, Abelisauridae, is represented, 
albeit questionably, iti the Campanian/Maastrichtian 
of Africa. Among crocodyliforms, Metasuchia, the 
caocodyliform clade that dominates in penecontem- 
poraneous horizons in South America, Madagascar, 
and the IiuHan subcontinent, is absent. Instead, only 
the neosuchian dyrosaurid Sokofosuchus is known. 
Among non-avian dinosaurs, there is oidy poorly 
preserved material, none of which is precisely 
identified; significantly, however, tio ornithischiairs 
are currently known. Campanian/Maastrichtian mam- 
mals have yet lo be discovered from rnaitdand Africa, 
although the possible gondwanatherian recently de- 
scribed by Krause et ah (2003b) could conceivably be 
from this horizon. 


d he record of terrestrial vertebrates from the latest 
Cretaceous of the Indian subcontinent has increased 
dramatically over the last three decades, largely the 
result of efforts Ijy Ashok Sahni of Panjab University 
(Chandigarh) and his students. The assend^lage, froirr 
below and interbeddecl within the Deccan Traps (the 
infra- and inlertrappean beds) was recently snmma- 
ri/ed by Khosla and Sahni (2003). The infra- and 
interlrappean beds are considered to be of late 
Maastriehtian age. The diversity of Lerrestrial verte- 
brates from the Indian subcontinent is low, and 
surj^risingly low in one clade tliat is diverse 
elsewhere, the Crocodyliformes. Two metasuchians 
(Baurusuchidae and Metasuchia incerlae sedis) and 
one neosuchian (Dyrosauridae) are present, but none 
of the metasLichian families identified in Madagascar 
(Notosuchidae, Peirosauridae, Trematochampsidae) 
have been definitively identified on the Indian 


* A possible gondwanatherian mammal was reeenUy 
describcul t)y Krause et al. (2003b), but the age of the 
horizon from which it was recovered is of uncertain agt^ 
within th{^ Cretaceous period. 


Annals of the 

Missouri Botanical Garden 

siihcunlmctil. N()n-a\ ian (liiiosauis were discovered 
oti [lie Indian siil)rontin(Mit om^v 175 vears a^^o. Maii\ 
specimens ha\e l^een dLsc()\ered since and deuioii- 
strale llial a diverse (anna exisled at Uiis lime. 
l'n(()rtuna(<'ly, however, few articulates! specimens 
1ia\(' been reco\ered and. as a result, ihe alplia 
taxonomy icmains amhiguous. Nonelheless, il is clear 
thai the most ciinimon (Hnosanrs [jreseiil at this time in 
achigascar (;il)fhsaun(l and noasaurid lliefo[)o(ls and 
ht host rot ian sauropods) \\c\e also preseni on llie 
luihan suheontinent. Hie nummialian fauna is repre- 
sented by fragnientar) isohited teeth llial ha\c been 
assigned lo at least three endieriart taxa (Decrano- 

Icsles, Sdhnilheriuni, and a ])()ssible olleslid) and 
a sudaniericid ^oudwanalliere (Prasad & Sahni, 1988; 
Codinot c^ l^rasad, 1994; I'rasad & Cothnot, 1994; 
Prasad el ah. 1991; Krause el ah. 1997b; liana & 

Wilson, 200:5; Khosla (4 ah, 2004). 

r I ^ 

alilc ( . 

(>r()C()(h hinriii genera f 

Kiiii [)ir-('aiii[iaiii;iii 
1 Ainciica. ^Vh ira. 

Pate (.a'ctaceous Ikji i/ons in South 

Anlafclica. and ihc Indian MihconUiirnl. hisl foi" Stmlli 

America compiled |»rimarily (ann Bcrlnii and Carvallio 

(P)90). an<l foi- Africa [inm MnlTctaul ( M>tl2) and Larsson and 
Gado (20(10). 

Sol Hi Amkhica 



.sucuci"(K'ou\ ua 

\'ofosti( hus \\ 



M(irili(fsuc!nis (iar\alh(> tK Hcrlim 

(A)n]<}lu(('sucliiis H()na[)arte 








Ijh\c()suc}tus Sliojiici 



Il is (dear, based on cni-renlb available saniples. 
ihal the grealesL simibull\ iii taxonumic compftsition 
of known Campainan/Maastrichtian teriT'strial vertt^- 
l)rale faunas lo that of Madagascar occurs in South 
yVmeriea and India. 


lliiiuiida^uchjis IJnl[i;tant 
". n s n c 1 1 i a 

SlonKilosiH-Jius Si rn iiicr 
ArgYpfosnchus Sh'inn cr 


No record 

1m)Ian Si i{C()\Ti\r\T 


o rccort 


PlU■:-CA.^^^\M A^ CriKTVCf.oLs ni^iiaiu rio.\ or 


A[NU Mammals ON (;()^i)\^A^A^ Landmassks 


\meriea, whereas lreuiato(diampsids. but not uotosu- 



^, are known h'om the pre-Campanian Pat( 

In ad(h[ion to compai"iii^ ihe laxonouuc composition (hclaceous of Alrica. Rolh notosuchids and tremalo- 

of croeod_\llfonTis. iion-a\ ian dinosaurs, and mammals (dKmi[)sids- as W(41 as the unjthiced mtdasu(diian 

from Catnpaniaii/Maaslrielilian Injrizuns o[ Madagas- AnirijK'suchus, are i-eeorded from Earlv (h-etaeeous 

ear. South AnKaica, Africa, Autarcliea, and the buhan hori/ons in both South America ami Abica. This 

subconlineni, il is rele\anl to record ila; pre- i-c\eals a deeper history on those landmasses, pie- 

Campaniaii Crelaeeous (hsiribulions of these same sumably jirior to se])aralion of th(^se huuhnasses near 

(dades on these saiue landmasses 

in order to 

the Parl\/Pate Cretac<M)us boundatA. P(drosauri(ls are 

potentially re\t'al deepci- hisloiies. As su(du Ta- known hnm the Early Cretaceous of Abica but not 
bles 7-9 provide an overview ol the generic (hversity Soulh America and b'oni neither laiidmass duiing the 
of (*roco{lyliforms, non-avian dinosaurs, and mauiinals pre-Campaiiiau Pale Cretaceous, [hdortimately, the 
from the pre-(^ampauian Pate Cretaceous, whereas record of identifiabh' pre-Campanian (h'etaceous 
Tal)les 10-12 pix)\ide the same information for the eroeod\ bforms Is nonexistent h)r Aniaietiea and tin- 
Early Cretaceous. Tlie j)re-(^ampanian Pale Creta- bahan subcontinent. 
eeous arid Ivirly Cretaceous distributions are listed 
!n(bvidually because there is general agreement 
among paleogeographers and paleonlologisis that 
South America and Ab'ica separated near llu^ I\arlv/ Piv-Campanian non-avian dinosaur faunas b-oiu 
Pate Cretaceous boundary (see below). Eatdi of the Condwana, parlicularly from Africa and Soulh 
clades will be considenMl in turn. 

NON-wiw DixosAi Ks cr\i!ij:sa. W) 

America, are gtaierally much bellcr tdiaraeteri/ed 
than iheir Cam[)anian/Maastri(dilian counterparts, in 
pari owing to ihe higher iucddenee ol hasin foj-malion 
(with concurrent seflimentation) duritig these titni^s. 
Notosuchids, but not trematotdiamp^ids. are known Ab(disaurids and lithosti-otians arc known bdm Africa 
from ihe pre-Cainpaiiian Pale Cretaceous of South atid South America during bolh ]irc-( ■.amj)anian Pale 

(:ia)(.;ou'i i ii uinis (ivta.Ks :. lo) 

Volume 93, Number 2 

Krause et al. 

Late Cretaceous Terrestrial Vertebrates 


lal.)le 8. Non-avian clinosaur genei'a from pi-e- 
Campaiiian Lale Crcta('cuiis liorl/ons in South America, 
Africa, Aiilaix-tica, and the Indian suLconlinenl. Lih^ls 
compiled From Weishampel et al. (2004), with additions 
from Gonzah'z Riga (2003) and Ajx^sleguia (2004) for South 
America antl Sereno et al. (2004) (or Afiiea. Qucbtion marks 
indicalt^ tentative phicenuait. 

Table 8. Continued. 

SoiTii Amkrk.:-\ 


Xenolarsosaiirus Martinez, Cimenez, Rodriguez & 

Veloclsaaras Bonaparte 

AheUsdunis Bonaj>arte & Novas 
Aucasaunis (^oria, ChJappe & Dingus 

flokelcsia Coria & Salgade 
Ah(4isauri(lae ind(^t. 



Aniksosdurus Martinez & No\as 


Giganotosaurus Coi'ia & Salgado 
Unenlagia iNovas 
Mega raptor No^'as 
Droniaeosauridae indet. 
Troodonlidae indet. 
?Ornithomimidae indet 
Tetanurac indet 
Theropoda indet. 


Amazonsauriis Carvallio, Avilla & Salgado 
Rayososaiinis Bonaparte 


Andesaunis Calvo & Bonaparte 

Argenlinosdunis Bonaparte & Corla 

ArL^yrosanrns Lvdekker 

Bonitasaura Apesteguia 

Epacthosd jirus Po u ell 

Mendozasaiirus Gonzalez Riga 

Tilanosauria indet. 



Rinconsaurus Calvo & Gonzalez Riga 

Lithostrotia indet. 

Neiupiejisdurus Povv(4l 


luropocia nu 



NolohrpsUophodou Martinez 


Anabisetia Coria iS. Calvo 
Gdsparinisaura Coria & Salgarlo 


Seceniosdurus Brctl-Sui'nian 
?Iguanodontia indet. 
Ornithopoda indet. 








Riigops Sereno, Wilson t^^ Conrad 

Abelisauridae indet. 

Dellddromeus Sereno, Dutheil, laroehene, Larsson, 

Lyon, Magwene, Sidor, Varricchio & Wilson 


Sigilinas.sasaurus Russell 


Sj)inosdurus Stromer 


Cdrchdrodonlosaurus Stromer 
Avetheropoda incerlae sedis 



Droniaeosauridae indet. 
Theropoda indet. 








cf. DicraeosauriLs Janciiseh 

Tilanosauria uicerlae sedis 

A eg ^ p I o s a I i rus S I ro n i e r 

Paraliutan Smith, Lamaiuia. Laeovara, Dodson, 
Smith, Poole, Giegengaek, Atlia 


Dicraeosauridae indet. 
Lidioslrotia indet. 
Sauropoda indet. 

cf. Ouraiwsaurus Tac^uel 
Euornithopoda indet. ^ 
Iguanodontia indet. "^^ 
Ornithopoda indet. 


Theropoda inrlet. 

h'tHAN SLBC(^N'^^K^"|■ 

41ieropoda indet. 

Sauropoda indet. (= Bruhathkdyosaurus Yadagiri & 


Draiidosaiirus Yadagiri & Ayyasami 

* hidicates taxa listed from only Marsa Matruh, Egypt 


Annals of the 

Missouri Botanical Garden 

Tal)lr 9. Matnnialiari ^rnrra from pre-Caiiipanian T.alc CreUiceous and Ivirly Cretaceous inl(M-vals, ihereby 
Ci(.'[accouy Iiorizoiis In Stmlli Anu'rica, Africa. Atilarclit-a. 
aiul []\r Indian sLibtonlinrnl. F.i^Ls compiled from Kiclan- 

indieatin^ iIk^ initial (liversifieallon (if these e 

Jaworowska et al. (2()() I). 

Socii! AMriiicA 

Mainiiialia inrlet. 


Maminalla indcl. 





ImM V\ SlliC()iMIM':M 


O fCCOI"( 


Tal)lc 10. CrococKIiiorni ^cncca (Vnm Earl\' Crctaccnus 
hoii/ons in South America. Africa. Anlarclica. a tit I tlic 
Inclinn snhcontinent. List for Scnilli Aiticrica compiled 
priuiaril) from Bertini and (larxnllio (1999), and lor- Africa 
from HnffctaLU ( 1 9o2) and l.arsson and 

Cado (2()()()). 

(^)ucstion mark indicates lental!\f jilacemenl. 








Cinididinlon (larvallio tX ('ampos 


AiJiargasiichns ('.\ui\\)\h\ 

?! rcmalocham[)si(hie 
Cdriristicbus KelltuM- 

Mcla>^nchia uiccrldc sedis 






Sdrcosiichus Marsli 
Mvndiosaanis Mones 






Mahiui'siu Inis jacohs. Winkler, ^o^^ tis tK" (lomani 
Aruitosiichiis S(M-cno. Sjdor. [-arjs.son & Cado 


Slolakrosuclius Larsson <S. Cado 

' Pre nia loci iani|)si( la^■ 






Mela^uchia inccrldc sedis 
ArdfipesiK hds 



N<M)snchia incerlar .sedis 

HrilldfKTdusuclnis Micliard. de Hioin. Hnmel tK ih 

No record 

Indian Si Bro\TiM;\'r 


io rccor( 


|>ri()r to tlie l>reakiip of Coiidwana. Noasaiirids are also 
known from AiViea (hiring these same inter\als, hul 
tlieir oeeuirenee in South America is linutetl to the 
pre-Campaniau Late Cretaceous, Tht^ pin logeuetic 
and)iguil} resulting from the relatively fragineiilary 

skeletal material of many of these taxa. parlieidarly 
noasaurids and lilhostrotiaiis, hovvi-ver, rKu-essarlly 
limits bioge()gra[iluc uderences (1eriv(*d from them. 

Similar t(* llu^ slluallou described al)o\(' for 
Campanian/Maastrichtian strata of tiori-Madagascati 
Coudwauan I and masses, pre-Caiii[)auIan (Cretaceous 
deposits, particularly of South Atnerica and Africa, 
also preser\'e di\erse uon-avian dinosaur faunas 
characterized by mnnerous clades of tclanuian 
theropods, uon-hlhostrntian saurcipods, ornilhopods, 

ankylosauiians, and slegosauriaus. I^atdcnlarl 

y pi 



lematic foj" Coudwa nan- wide biogeographic recon- 
structions is the \ irtual absence of Earl) Crelaect)us 
dinosaur diseo\er!es from Antarctica, India. an<l 

[VlAMMAt.S (TAMI.i;S <J, 12) 

None o( the low(M'-level mammalian taxa n^coviN'cd 
from the Maastriidiliau of Madagascar are shai'cd with 
pn^-Camj)anian (!retaceous linrizons from odit^- Cond- 
wanan laufhuasses, l)ut the biogeographic rtde\ance of 
this information is hniiled by the extrenndy j)()or 
knowledge ol ihe nuuumalian fossil record for the 
entire Cretaceous of Condvvana. Willi ihc |>ossil)le 
exceptions of a caudal vertebra from Libya (Nessov et 
ab, 1998) and a dentary fragment fioni Iba/il (liertini 
et ab, 199,"5). both (tfwhiidi were recovered fi'om poorly 
age-constrained horizons (Santonian-(>ampanian), 
there arc no known [)re-C]ampanian Late Cretaceous 

mammals known from Condwanan land masses. In 
addition to an important assemblage from Australia, 
Karly Cretaceous Condwanan mammals are known 

only from Africa and Soutli Ameiiea. A Barremian site 
in Cameroon has yi(dded evidence of at least three 

nontribosp)henic iherians, only one of whicli, the 
peramurid ''euj}antotherian" Ahclodon^ has been 
named (Brunei et ab, 1990). By contrast, a di\crse 
manunalian fauna of Bcrriasian age has been re- 
covered from Morocco and includes eutriconodontans, 
archaic *'s) mnietrodonlans," "en[)anlolheriaus."" and 
''iriboiherians'' (Sigogncau-Russell et ab, 1998). A 
lale Hauterivian or (\nly Barremian site in Argentina 

has yielded mnnerous skeletal remains 


r ii 


/atherian Mncrlrsh's (e.g.. llopson <_*<. Hougier, 199."^), 
l)ut this is the onl\ South An 

jcrican manin 

al sit 

e o 


d(diniti\e Latl_\ (Crrlaeeons age. 

Volume 93, Number 2 

Krause at al. 

Late Cretaceous Terrestrial Vertebrates 


'rii[)le 11. Non-aviari dinosaur genera 

from Karlv Tnhle 1 1. Continued. 

(^riMaceous horizons in Soulh America, Africa, Antarctica, 
and the ln<lian snheontiiicnt. Li sis compiled from 
Welshampel el al. (2004) with adch'tions frotn Leanza el al. 
(2001) for South America and Sereuo el al. (200 Ij for Afi-iea. 

Sot ]ii Amkhica 

Ijifdhjieino Bonaparte 

Ceralosauria indet. 
Aln'lisauri(la(^ indel. 



Jrritalor Marllll, Cruicksliank. Ficv. Small »X: 

Angalurama Kellner & Campus 


Careharodonlosanridae indel. 

Santdnnraptor Kellner 
Coni]iso<^nalhidae indel 
()\ ii-a|il(jrosauria Indet. 
'rherojjoda indet. 



Afudrgasannis Sa1^a<lii i.^ Bonaparte 
I'chhaehisauridae indel. 



Agustinia Bonapnrle 
ChuhutJsaunts d(4 (^orro 

Tilanosauria indet. 


Slegosauridae Indet. 

Iiruanodontia indet. 
OiTiidiisehia indet. 



Spinnstrophejis Sereno, Wilson ik Conrad 


Noasanridae Indet. 

Al)elisauridae indet. 


AJrorenafor Sereno, Wilson, I.arsson, Dulheil & 







SucJiomimus Sereno, Beck, Dullu'il. Gado, Larsson 
Lyon, Marcol, Rauliut, Sadlier, Sidor, 
Varrleciiio, \\ ilson & \\ ilsun 
Spinosauridae indel. 



CarcharodonlifSduriLs Slronier 
Avelheropoda utccrtac scdls 





Coelnrosauria inceriac scdis 

Nrpvehasaurus de Klei'k. Forstisr, Sampson. 
Chinsamv & Boss 
Tetanurae indel. 
Theropoda indet. 



Nigcrsaurus Sej'eno. Beck, Diitlieil, Larssun, Lyon 
Moussa, Sadlif^r, Sid(»r. Varricchio, Wilson t^ 



Rehhachisaiinis ]>a\'ocal 
Uiplodfx idae indel. 



Jolxirid Sereno. B(^ck. DuHum"!, Lai-sson. [.von. 


Sadlier, Sidor, \'ariicehio, Wilson & Wilson 


Brachiosiiuriis ni":irs 



Med (I 


Lilhf)strolia indel. 
Sanropofla indel. 


Ank\ losauria 

Modosauridae indel. 

Baraiilliodoii No]>csa 
Thyieophoia indel, 

Lurdusdiinis Ta(]uct t\ lUissell 
\aldosaurus Gallon 
i ladrosauridae 
Ignanodontia indel. 
Oriiilhisehia indet. 



o recoi 


Indian Si ucominem 

No recoi'd 



o reeori 



Current evidence suggests a numl^er of (dose 

lnoge<)gra})hie ties linki 

ng pre-Campanian 



fninias from Afriea and Soulii America. However, il 
must he noted that data lo evaluate faunal links with 
oilier Gonduanaii Ian(hnasses, incducUng Madagascar, 
are minimal. The undeserihed fauna! assemhlage from 
the Aiika/omihaljuka satidslones (Curry, 1997; Curry 
et ah, in prep) may have a significant bearing in ihis 



Annals of the 

Missouri Botanical Garden 

Tal)l(^ 12. Mnrnrnaliaii getirra from KarK (a'<'tac(M)i]s 
luiri/nds in South Anif'i"ica. Alcica, Aiilanlica, and llii' 
Indian sulx-onlincnl. conipiled trom Klclan-Jawoiow^ka 
el al. (2001), uilh addilion.s ftojii ilain] and llalin (200:]). 
Qui'SliiHi mark indicalcs Uailalivc [)lar('niciit and (jnolation 
macks iiidlcalc paiajjlnlclic taxa. 

SoL/rii Ami:i;h.a 




Vnu'clrsl !da(* 

]^inc('lrsfrs IJonapailr 




Fatiii1\ in(.aa"lac scdls 

( Jcnus indcl. A 

(irims indcl. R 


(wMiiis indrl. 

I''atnil\' indcl. 


l)yshri(i)il<)!i Stgognran-lviisstdl 
ichth vocontxloii Si^io'incaii-llussi 
I lahnodutilitka.' 

DvmsodoK Ilaliii ^K llalin 
lltfliii(>ihni Si^D^iu'au- Russell 
r,cnus indrt. 

Afclialc "s\ mmctiodnntans 
K;imil\ indcl. 


\fltis()(l()!} Si<r()o;!n\ui-l{usstdi 
iMnnx/rrson Si<^0i*;m'an-Rlissf 





llicrctiodon SIgogn can-Russell 
Slem (.".ladollieila ('^aipanlollua-ians" 
l''aniil\ indel. 




Ajruiuminus Si^()nnt'au-Rus>( 
Minimus Sim tunean -Russell 

A ' %. 



i)(H\t)<l()t\ St^d^neau- Russell 

AhcliidiH! Rinnel. (.oppeiis. Ijejav. I'UnrK Ik^inl/. Il< 

JMfohs. jclifUfii', iMouelielin, Pillx'am tS. Sudi'f 


iiniiis \ iwen 

Stem H(H'eesp|](aiida 


llyponi) lo.s Si<^ogneau-Russell 

Family indel. 

Trihifllu-riuin Si^o'i.neau-Ru.ssi.'ll 
Am AiiciicA 


() ieeor{ 


Im)1a\ St ii(:(),MiM':N'r 

No reeonl 

Pini.OGKN^ AMI L]i()(;K()(;R\]'in 01 I. All: Ckkivckols 

(jiOCODM.II-OliMS, N(),N-Am\N I)|,M)>\IKS. 

\\n \1am\i\i.s riiini M \nA(;\srut 

Of llie seven fatnil) -h^vel laxu of crueocMifoniis, 





noti-avian (iniosaiirs, and niaimiiais Known ironi me 
MaastfieliLian of Madagascar, all are shared wilh 
Canipaiiian/Maaslricdilian fannas of Soiilli Aniei-iea. 
Tins is suggesli\f^ of elose hiogeographie lies and, 
iiuleed. a degree ofeostnopolitanisni lliat is diffienii to 
e\j)lani in llie eoiilexl ol most ['ecent juileogeographic 
reeoiistruelioiis depleting .^epaialion o( most Condwa- 
nan landniass(^s l}v i^n^al distances at (his time ((\";.. 
Lawver et al.. 1992: Snnlli et al.. 1991; Reeves & de 

WiU 2000; Maiks cK Tikku, 2001; Rolslein el al., 
2001; Scotese. 2001; CrNcill et al. 2003: de Wit, 
2003; Bernard et al.. 2005). Aeeoj-ding lo these 
reconslruetioiis, Madagascar had long Ixhmi isolated in 
the Indian Ocean by the Cain])anian and, nu>re 
s])(^(;ilieally, an) t<M-i-estrial conlinuily with Sonlh 
America, by whatever I'oule, had been sevennl some 
50 million years earlici\ H(»we\er, the nM-ord of Late 
Cretaceous terrestrial \crlebratcs from (^mdwana is 
spotty at besi and thcicf((r(^ ditTitadl to interpret in 
a biogeographic c(jntt^xt. 11 ic best possibilities for 
obtaining a bioge<»graphic signal come from crocod\]i- 
fornrs, non-a\ ian dinosaurs, and mammals, in |)art 
])eeause of (heir relat i\ cK good pi'esei'valion and 
therefore relati\<dy pr(H-ise identification, and in [>art 
because they are relati\e]y widl-studied. Indeed, the 

■ks. 1 

wo monumcniai worKs, ny 

recent pu])licati()n of t 

Weishampel et al. (2001) on dlm^sanrs and Kielan- 

jaworowska et al. (2()()1) (»n manmials, facilitates Uie 

compilation of ocenirence data that are used lutein lo 
reveal dislribntional |^atlcrns for these taxa. Here we 
document llie a\ailablc taxotiomlc atid phvIog(Mi(^lic 

information that mlglil ha\t' a more immediate bearing" 
on our understanding of Oonihvanan biogeography. 


Ph}logenetic analyses ha\ c bciai presented for only 
three of the seven species ol crocodylilorms known fn^m 
the Late Oretaeeons ol Madagascar. The [)hylogenetIc 
relationship o( MahaJdii^-asuchiLS itisiij:f}i.s lo other 
metasutdnans was examintMl bv Ihicklev and Broclin 
(1999) and Buckley et al. (2000). These analyses 
indicated a (dade that consisted of TreuKitochampsa + 
Mdhajdngdsucluis + l\arosauridae, Avitli Araripcsuchus 
l)asal to this elade. This result tends lo suppt)rt the 
c(>ntenlion of Buflctaul (P><)!i. I*)[!0j, wjio argued that 
Peirosaundae should be considered a juni(jr s}'nomni of 
I reniatocdiam[)sidae. W illiout more conchisi\ e evidence 
and a more thorough undcrslaiiding of trematoehampsid 
taxa, iVIahdjdfigdSiirlnis was (dassilicd as Metasnchia 

Volume 93, Number 2 

Krause et al. 

Late Cretaceous Terrestrial Vertebrates 


incertac sedis. Tykoski el al (2002) and Turner and the Peirosaiiroidea. Il is likely thai diese discrepan- 
Calvo (2005) ol>lained identical results to Buckley and 

cies cire due to tlie authors' reweighting of characters 

Brochn (1999). Carvallio el al. (2004) did not include hased upon rescaled values, a practice uol followed by 
any traditional treniatochampsids in llicir analysis, but other studies. 

A recent biogeograpliic study by Turner (2004b) is 

found MahajaugasucJiiis to be embedded within the 
Peirosauridae, with Uberabasuchiis Carvalho, Ribeiro & 
dos Santos Avilla from the Late Cretaceous of Brazil as crocodyliform distribution. Turner (2004b), employing 

highly relevanl to the question 

of Cretaceous 

its most closely related sister taxon. 

a time-slicing protocol adapted from Upchurch et al. 

Buckley et al. (' 

determined that Simosuchus (2002), conducted a cladistic biogeographic analysis 

and its closest sister taxon, Urugudystichns, from the of a diverse sample oi Cretaceous crocodyliform taxa, 
Late (Cretaceous of Lmguay, formed a clarlt 

; wiin 


mostly from Condwana. Liclnded in his sample Avere 
M alawisuchus , and that these three taxa were question- three taxa known from the Late Cretaceous of 

Madagascar: Simosiichus clarki, Mahajangasuchus 

able members of the Notosuchidac (which included 

Notcisuchus + Lihycosiichus in their analysis). This insignis, and Araripesachus sp. indet. The sister taxon 

relationship was supported by several subsequent of SimosucJuis in Turner's analysis is the Late 

analyses. Tykoski et al. (2002) recovered a nearly Cretaceous South American form Uniguaysuchus, 

identical I 

icai iree, wnn ^ 

ith Simosuch us and Uruguaysucli us 


nis supp 

ortimi an earlier assessment ])\ Buckley et 

linked as closely related sister taxa within a notosu- al. (2000). Turner resolved a sister taxon relationship 

chian clade. Sereno et al. (2003) placed Simosuchus between Mahajangasuchus and the South Amei'ican 

within the Nolosuchia (including a Comahuesuchus + Peirosauridae, which also supports the earlier analy- 

Analosuchus clade and a Simosuchus + Araripesuchus + ses of Bucklt^y and Brochu (1999) and Buckley et al. 

traditional sebecosuchians + Malawisuchus + Notosu- (2000). Araripesuchus sp. indet. occurs at the base of 

chns clade). Tree to]>ology regarding this clade is nearly a clade of other Araripesuchus species from both 

identical vviUi the earlier study l)y Buckley et al. (2()()()), Abica and South America. In his analysis, Turner also 

with the exception of the exclusion of Araripesuchus included Pabwehshi, a yMaastrichtian mesoeucroco- 

the Indian subcontinent recently de- 

Ironi the Notosnchia. Sereno et al. (2003) additionally 
recognized an expanded concept of Notosnchia, 

] \ ban f ] 

(jyiian irom me incnan 

scribed by Wilson et al. (2001). Turner 

roughly equivalent to the Zipliosuchia proj)()sed by confirmed Inclusion of Pa/>icc/z.s7u" in the Baurusuchi- 

Ortega et al. (2000), by including Comahuesuchus, dae, othenvise only known from the Late Cretaceous of 

AfialosucJius^ and Baurusuchus + Sehecus Simpson. 1\)1 Brazil and Argentina. Late Cretaceous crocodyli(orms 

(2003) recovered a tree similar to those of Buckley et from the Indian subcontinent are poorly known, based 

ab (2000) and Sereno et al. (2003), with Simosuchus almost exclusively on isolated teeth (Prasad & de 
fii-mly nested within Nolosuchia. The constituency of Lai^parent de Broin, 2002). However, based on 

available information. Mala^^asv and Indian crocodvli- 
forms share closest affinities with roughly contempo- 

his notosuchian clade strongly reflects that proposed by 
Ortega eL ai. (2000) and Sereno et al. (2003), with the 

Iv k 

oniv Kev ( 

lifference being the exclusion o( Araripesu- raucous taxa from South America. 

chus, as was also proposed by Buckley et al. (2()0()j. It is 
worth notin- that Ortega et ab (2000) and Pol (2003) 

Turner (2001b) refined the methods of Upchurch et 
2) and revealed two (:ontinent-leveI vicariant 
include several taxa not included in the oilier two events: (1) separation of Africa, South America, and 
analyses, resulting in a more geogra[)liically wide- Indo-Madagascar from other non-Condwanan land- 
spread notosuchian (or zlphosuchian) clade. These taxa masses earlier in the Cretaceous, and (2) separation of 
include Chimaerasuclius Wn, Sues & Sun from the 

-\frica from South America and Indo-Madagascar later 

Early CnHaceous of China and Iberosuchus Antunes \n the Cretaceous. Turner (2004b: 2007) states that 

from the Paleogene of Ku rope. Turner and (^alvo (200. >) ^^[l^i^ later event depicts a rather non-trad I tlonal 

essentially mirrored the earlier results of Buckley et al. l)iogeographic relationship and, in that respect, this 

(2000) iji producing a Malawisuchus + Uruguaysucli us study's results are similar to and support tlie 

-I- 57mo,si/c/7?/.s' clade within the Notosnchia. conclusions of Sampson et ab (1998), Buckley and 

The most contrary hypothesis regarding the re- Brochu (1999), Krause et al. (1999), Krause (2001), 


and the geological data of Hay et al. (1999)." 


lationship ui' Simosuch us to other mesoeucrocodyliau; 

was put fortli by Carvalho et al. (2004). They placed 

the genus, along with Chimaerasuchus. within the 

Chimaerasuchidac, a clade basal to their Notosuchi- 

morpha. Other differences also a[)pear in tbeii- results, 

including the exclusion of Uruguaysuchus from the perhaps better suited than crocodyliforms lor re- 

N<jtosuchia and the placement i)[ Malawisuchus within vealing biogeogra[)hic pattern as it relates to subaerial 

It could be argued that non-avian dinosaurs are 


Annals of the 

Missouri Botanical Garden 

landinasses, because lliey were likely more closely of Morocco, \\1ieii originally descrihcd hy Sampson et 
licfl lo the Icrrestiial realm. Moreo\(M\ most taxa were al. (2001) and Caiiano et al (2002). the relationsiiips 

very lar^e. making il It^ss likeN llial du:\ would have 

been able lo rafi across great dislances 





mats of \egetalion. as has been documented for 

of Mdsidlidsaurus wevc also unresohed. althoudi it 
was recognized thai its affinities la) most (dosely with 
NodSdurus, Ldrrlsuclnis, Geriusdiirus Acearie, Bean- 
smaller-bodied exlant vertebrates (Censky et al., doin, Dejax, Fri(^s, Michard & Tacjuet, and llokelcsid, 
1998). As ior crot'odyliforms, the majority of non- and sei-ondardy with the abelisanrids Majimgdtholus. 

(Airnntaurus. Xenoidvsosdunis, and Abctisdiirus. Addi- 
tional remains ai Masidhcisdurus reci)vered during the 

avian dinosaur taxa known from the Late Cretaceous 

ol Madagascar share fdosest affinities with penecon- 

lcm[Joram'ous laxa from South America and India. 2003 field season ^irc current!) und<'r >lud\ by M. 

Preliminary [.Itylogenetic analyses have been pre- Carrano, S. Sanqtson, and M. Loeucn. hi a preliminary 

sented lor all (oui of llie saurischian taxa known fn>m re|)ort, Carrano et al. (2001: 44A) regard llie 

Madagascar (Sampson et al., 1998, 2001; Curry Noasauridae to lie abclisauroids ^trom llu^ Cretaceous 

Rogers & Forsler, 2001, 2001; Curry Kogers, 2002, of Ajgentina (NddMwrus, Veloclsdnrus). India {Lieri- 

2005; Carrano el ah. 2002). 

suiluis). Madagascar [Mdsiakdsdurus), and possibly 

Majtnigalhdliis^ an abelisaurid, has been included Europe and Africa." 

in se\eral recent |)h\ logenetic analyses. Sam[)son et al. 

Rapclnsdnrus has been incduded in s{n'cral pinlo- 

(1998) ])la(^(Ml this Malagasy abelisaurid in a polytomy genetic analyses, the most compreli(Misive by Curry 

with Indosdurus and Indosachus from tli<^ Maastrichtian Hogcrs (200S), but also by Curry F^»g(a-s and Forstcr 

of India, Ahdisdiinis from the Sanlonian of Argenlnia, (2001) and Wilson (2002). All three of these analyses 

and Car//o/^////i/.v from the Campaniau-Maastrichtiau of agree in their resolution of a dose reIalionshi[) 

Argentina. Relalionshi])s within this |)olytomy were In'tween Wcnicgfnsdiirus NoMinski from ihc Cam[ia- 

'what luster ri^solved by Sampson et al. (2001) and nian-Maaslrichtian of Mongolia and Rnpclosaurus, but 


Carrano et al. (2002), who posited dui( Majiingatholus postulate different successive oulgroui): 

s atui Close 


and Cdrnoldums were sister taxa and that they, relatives. Curry R.)gcrs and Forstcr (2001) and Curry 

togctJier, were the sist(a- laxou of AhclLSdiirns {hi- Rogers (2005) identify a clade thai includt^s ;l/r//r//r/;- 

(losdiirus and Iddosiicliiis w^ere not included in the sdiinis from the Aplian of Malawi and ^(n'eral ta\a 

analyses). These results were in essence supported in from India and/or South America (e.g., /l///f/rr/a^r/?/n/.s-. 

a more cottipR^bcnsixe analysis by 'lykoski and Roue Agustinid). Wilson (2002) instead Ideiilifics Mdhuil- 

(2004). Coria et al. (2002) group(Ml Mdjungdtholus with .sa///7/.s- as a more basal bdiostrolian. with Rdpciosdiims 

AhdiSdurus and lldLclcsid in a poKlomy that com- ^s the sisler laxon to a clade of mon^ derived 

prised die sister taxon o{ Aucds<nirus + Cdvnotdunis. titatiosaurs iiudnding hisdiiras cdlhrrU Jain & Ban- 

India) and Saltasauridae (including laxa fnaii Nortl 

Wilson et ab (2003) descrijjcd a new abcbsaurid, dyopadhyay (from the Campanian-Maaslrichtian of 
RdjdSdiirus. from the Maastrichtian of India and 

reported resnils of another cladistic analysis of Amia'ica, Mongolia, ami South Anu-rica). 
abelisanrids (later presented b> Scrmo v[ ab, 2001), Malagasy Taxon B has recentl) been Includt^d in 

hich concluded ihal Ahelisdurus,, Rdjasdums, and a more comi^relienslve analysis of lilanosaur i>hylog- 



eny (including over 29 pnri>orle(l t ilanosaunans; 


MajungdtholiiS + Cdrnolaurus occnpictl successive 

nodes on a tree. The later sludy b) Scrcno et al. (200 I) (;u,-,y Rogers, 2001. 2005); die strict cons(>nsus tree 
also included a innvly named Cenomanian abelisaurid dearly resolves it a> nested Avithin the Saltasaurinae 
froni Africa, /?//-o/>.s fref(aTe(l t.) as "Niger taxon 2" in (sensu Wilson .K rpchurch, 200;]). Saltasaurim'.. 
Wilson et ab, 2003). Most significantly, tles])ite the 

sliuining positions among ^.,. ..., j^ 

analyses have concluded thai the (dosest k 

ab(disani"id trtmcra, all 

traditionallv intdude onlv three South American 

genera {SdUasdurus, Ncuqurnsaunis, and RocdSdiirtLs) 

and arc uui<niel\ charactej'ized b) the piesence of 
relatives of Mdjiingdlhotus lie in Campauian-Maas- strongly procoelous, dorsoventrally compressed distal 


tricbtian lioii/ons ol Argentina and Iiulia. 

caudal vertebrae. 






M \M\I \I.S 

Most of the mammalian laxa from tl 




iinis IS currentt\ considereft to ne 
a noasaurid abelisanroid (Carrano et ab. 2004: Scrcno 
et ab, 2004; Tskoski & Uowe, 2004-). An aiialvsis bv 
Scrcno et ab (2001) conckuhMJ thai MdsiakdSdurus 
lies in an uiucsobcd polytomy with Nodsdiirus from 
the ?late Campanian-Maastri{ditian of Argentina, an 
unnamed genus from the Aptian-Albian of Niger, and 
Dclladromeus (originally regarded as a basal coelur- laxonomic level. oi- bccairsp the taxa n'pn^sented are 
osaurian by Scrcno et al., 1996) from the Cenomanian unknown from an\ other landmass. Such is elearlv the 

Cretaceous of Madagascar provide liitic biogeograplht; 
information, (nlher Ixn-ause the sjiccimcns are loo 
fragmentary to pertnit identificati(ni t(t a lower 

Volume 93, Number 2 

Krause et al. 

Late Cretaceous Terrestrial Vertebrates 


case for ono isolated looth of a large taxon and for et al., 1992). Most workers (e.g., Lawver et al., 1992; 

a nearly complete skeleton (Krause, 2003a); both taxa, Miiller el al., 1993; Roeser (^t al., 1996; Marks & 

if they are different, eannot be idenlified as yet Tikku, 2001; Coffin el al., 2002; Kent el al., 2002; 

beyond Mammalia incerlae sedis. O'Neill et al., 2003) posil thai a through-going seaway 

The presence of gondwanalheres, however, is intervened between Indo-Madagascar and Anlarclica- 

imporlanl. The two [ccih questionably idenlified as Australia by the mid to late Farl\ Cretaceous (130- 

gondwanalhcrian are relativ(;ly uninforiTialive, but the HO Ma) and ihat subsequent spreading between these 

two sp(^ei!n(ms ihat have been assigned to Laranify landmasses proceeded rapidly. St^veral recent palco- 

miotaka, a sudaniericid, provide important biogeo- geographic reconstructions, for instance, illustrate 

gra[)hic dala. Su(kuii(Micids are elsewhere known from a separation betw^een Antarctica and Indo-Madagascar 

the Late Cretaceous and l^aleocene of Argentina, the of approximately 950-1100 km (employing 111 km/ 

Late Cretaceous (Maastrichlian) of India, and the degree of latitude conv(nsion) by 96 Ma and 1700- 

Eocene of Antarctica. Laranify appears to be most 1850 km by 83 Ma (Rotstein vX al., 2001: fig. 9; 

closely ndated lo the unnamed sudamericid from Bernard et al., 2005: figs. 4, 5; ScIkMHuo & Scotesc, 

India (Krause et al., 1997b). 

Pai.k()(.eu(.uaimiic Kt^coNSTin;cTioNS: Wt:rn': South 
Amkiuca anu Mauacascar CoNNK.crKi) in TUt: 



2005: figs. 4, 33). In pari lo reconcile the develo[)ing 
record of vertebrate fossils, Hay <'l ah (1999) boldly 
proposed an "alternative global ('relaceous paleoge- 
iiphy" in which intiMinithMit land connections 
persisted between Indo-Madagascar and yXnIarctica, 
across the Kerguelen Plateau, w<dl inio the Late 
Cretaceous (perhaps as late as 80 Ma). Case (2002) 
Eastern Hemisphere and South America's location in also proposed a persisLciit land bridge, allhough 
the \\est(M-n llemisplicre, and despilc (hffcring details farlh(T west, across the Gunnerus Ridge and Kainan 
in flepictions of Condwanan paleogeography, it is Maru Seamount. 

clear that the t\No landmasses were much closer to one Finally, in th(^ mid Late Cretaceous, another major 

another in the Mt!so/oic than they are today. Pricjr to rifting t^vcnt linked to the Marion hotspot led to the 
the break-ui> of Pang(>a, a non-o])strucled (by oceanic separation of Madagascar and ln(ha. This episode of 

Despite Ma{higas<ar's current position in 


straight-Hnf; distance bi^lween Soulh Anun'ica and 
Madagascar is almost {)()0() km. Wilh the fragmenta- 

waters) o\erland route across Africa s|)anning some seafloor spreading was accompanied by an outpourin 
3000 km separated ihe two areas of interest; today the of flood basalts on both landmasses. Dates (roni these 

basalts cluster in age from approximalely 91 to 84 Ma 
(Storey et al, 1995, 1997; Torsvik et al., 1998, 2001). 
lion of Condwana, which is generally agreed to have Wilh this final episode of Late Cretaceous rifling, the 
conunenced in earnest in die Late Triassic lo Earl) Indian subcontinent moved rapidly northeastward 
Jurassic (Lawver el ah, 1992; I'orsvik et al., 2001; de toward Lnrasia (Puunhianasolo et ah. 1981; Storetvedl 

Wit, 2003; Wells, 2003), Madagascar, as part of ^1iasl et al., 1992; Storey et al., 19<)5, 1997), and 

Condwana'' (also including the Indian subcontinent, Madagascar, situated several hundred kiU)mclci-s from 
Antarctica, and Auslralia), began to separate from mainland Africa across the Mo/ambi(iue Channel, has 

remained isolated in the Indian Ocean ever since. 
Rifting in "West Condwana'' between Soudi 

''West (TOJidvvana'' (Soulh America and Africa). 

Initial lifting between the Indo-Madagascar block 

and Africa began during the Permo-l^riassic, and America and Africa commenced 





seanoor spreading belw^een the conjugate-rifled mar- Cretaceous, and b> a[)pro\iniat(dy 120 Ma an ajin of 

Kenya, and Tanzania the South Atlantic extended well norlhward between 

gins of southern Somalia, 

(Western Somali liasin) and northern Madagascar the two landmasses (Law\cr et al., 1992; Miiller et ah, 
commenced by the late Middle Jurassic (Lawver et al., 1993; Smith el al., 1994; Scolese, 1998: Hay el ah, 
1992; Wells, 2()0:]). 15) the Late Jurassic (approxi- 1999). Geophysical dala indicate that a ihrongh-going 
rnaUdv 160 Ma), a narrow seawav separated the east seawav inlervened between Soulh America and Alrica 

by the beginning of the Late Cretaceous (Niirnberg & 

East Conduana 14oc k. During the Late Jurassic, Lido- Miiller, 1991; Lawver el al., 1992, Miiller el al., 1993; 

Plelsch et ah. 2001), and normal mai'inc communica- 
tions, as e\idencc(] bv the distribution of Cretaceous 

coast of Africa h-om Madagascai" and the rest of the 

Madagascar shifled southward along the Davie 


Zone, uhimatclv coming to rest some 

400 km off the (^ast coast of Mo/ambi(iue in tlie Early echinoids and fishes (Maisey, 2000; Neraudcau & 

Cretaceous (130-120 Ma). 

Mathey, 2000), uere apparently established between 

At about this same lime (mid Early Cretaceous), the Western Tclhys and the South(M-n Ocean domain 
seafloor spreading commenced between the Indo- by approximately 100 Ma. The Antarctic Peninsula 
Madagascar block and Antarctica-Australia (Lawver and South Orkney group remained contiguous with the 


Annals of the 

Missouri Botanical Garden 

soutlirni ti|» of South America lliroii^liout the \ /Mr. and South Amoi-icn duritig (>ainpaniaii/\laastri('htiau 

Cn'Iac(^()iis and well iiilo [he derliary (La\\\'ei- ct ah, limes are not kno\vn fiXMU j}eneeontemporaneonr. 

1992; W(K)dl)ui-ne cK (^ase, 1996; Hav el ah, 1999; horizons in mainland Africa or. (or thai matler. 
Regnero et ah, 2002; Lawver & Caha^an, 2003). 

There remains strong iudicalion tlial Africa was llu; 
first major hmdmass lo hecorTie isolated hy eireum- 

Anlarctica. Nonetheless, des[)ile llit^ inhMisity of 
reeenl exploration and collectini^, llie fossil ret;()rd is 

nol fully up to the task of testin^^ whether or nol this 

continenlal seaways during llie hreakup of (^ondwana. |)allern is real, a point made repeatedly hy our 
with holh g<M)physieal and hiogeographie data sug- working group and others (e.g., Krause et ah, I997h, 

the end of the Karly 1999; TorsU-r, 1999; Rogers el ah. 2000; Carrano cL 

g(^stive of isolation heforc 

Cretaec<His (approximately 100 Ma). Whedier or not ah. 2002; Lamanna el ah, 2002; Krause, 20(nh; 

indo-Madagascar maintained interniitteni eonu<M'tions 

O'Connor el ah, 2006). The geologic slag<'s ol the 

ei'resl rial fossd 

with Aniarctiea \ia the K<?rguelan Plateau (Hay et ah, (jclaeeous foj- which the records of I 

1999) andAtr tlu^ (innnerus Ridge (Case, 2()()2j inti) xerlehrales from Madagascar, the Indian suhconti- 

ihe later stages of the Late Cretaeeou: 

s remams 

neiil. and South America ai'c rtvisonaliK well samph'd 
dehataltle. Kaimal data described in thi> leport are, are, for the most part, the very stages I'm wliich tlu^ 
ho\ve\('r, consisl(Mit ^\ith a scenario ol fauna! in- African record ]^ poor, and \ ice versa. As cmpltasi/ed 
lerchange among "East Condwana'' landmasses (Ma- hy Krause el ah (1999: 6). ^one of the ke\ stumhlin 

- - . is llie \ irtual lack of UM'i(\sli'ial atul 


dagascar-lndian suhcontinent- Antarctica) and Sctuth 
America until late ni the Cale Cretaceous (see l)elou). fre^hwalet vertebrates hom die post-(;cnomaniati 

I of 

ossit recoix 

(-o\n\\ \^\^ h'tj \<,MtvNT\Ti()N am) Latk 
C[ii';r\(.j':(K s RiocI'Ociiai'iiv 

l.ale ('relaceous of Africa.'' Tlie 
lerr(\strial vertebrates from mainland Alrica i; 

s miicn 

better for llie Karly (a't^taeeous and pre-( !am[)anian 

[.ale (ax^aceous than it is for the later staj^cs of ihe 

I'ragmentation of the Condwanan su|iercontiruMit hate (a-etaceous, whereas llie revers*^ is true h)r iIh^ 

and dis[)ersion of its constituent landmasst^s during otluM- three landmasses, parlicularly Madagascai- and 

the hilter liall of ihe Mesozi 



ra inidoiUHediv na( 

the Indian subcontinent. To further eompbcale 
jirolonnd effects on resident faunas of lerrestrial mailers, the record of terrestrial \frtcbratc fossils 
v(M'lel)ratcs and llicii- subse(|uent (Holutionar\' hist(»- from the Cretaceous- of Antaiclica remains all 





ries. Combining geophysical and straligraphlc (hita fot 
Condwanan breakup with obser\ations of famial 
distributions pro\ ides an unprecedented oppoitiniit) 
lo rev<'al larg<-scah' biogeogi-aphic palterns. llowe\er, bi(tg(-ographic hypothescvs (Fig. 8). d1ie firsl. rectaitly 

in\oking (Vlcris jxirahis, there is no reason lo assume h)inmhited and hibeled the ^'pan-C/oiuhvana" h\[>oth- 


This unc\cn leni[)oral .sampling has inlnhiled, and 

compet uig 

delinitive testing of luo 

geologic data, by th(Mr \'ery natnre. hold priority 

esis by Sereno et ah (2001), sli[iiilates thai \arious 
chides of terrestrial vertebrates were broadly distrib- 
ai-e rarcl) e(|uah LlnhMiunately, for the Crelaceous of uted thrt.iighoul Condwana during the l\arly Crela- 

o\('r j)aleontol()gic data or \ ice versa 

■yet all things 


ondwana, srddom are both the 

geologic an< 

ceous and that the much more limiled distributions in 

palcontologic dala sufTicienl for specified lemp(iral the p(Ksl-Cenomanian Lale Cretaceous (including in 

slic:es and geographic areas. For some times and Africa) iwc the result of poor sampling and/or 

places, the geologic data suppoiting ])aleog(M)graphic diHcreutial extinclion. A corollar> of this hypothesis 

reconstructions are sound, plentiful, and (lcri\("d fi-otn slat<^s lliat land connections belwetMi (1) Alrica and 

independeni sources, and resulting inteiprelat ions South America, (2) South America and Antarctica. 
Iiave been made u Itli confiilence. For otlu.a' times and 
places, the h)ssils are numerous, -well pres(M'\ed. and 

and (3) Antarctica and Indo-Mada^rascat 

were a 


tlunng a re 

lati\tdv brief inteiAal al the 

have l)een incorporat(Ml into rigorou> f)h\ logenetlc bcgitming of the Lale Cretac(M)us (ca. !0()-90 M)r 

frameworks. In this regard, the devtdoping Crelac(M)us ago)" (Sereno et ah. 2001: I;i28). Implicil In this 

record n\ lerrestrial vertel^rates from C/ondwanan h\pothcsis, dicrtToRs is the pr<MliclJon tlial terreslrial 

landmasses is beginning to [)ro\ ide an opportimltv lo veitebrate faunas on eacli of these major landmasses 
furl her clarif\ the timing and sequeni-e of ( loud w a nan 
(ragmenlat ion. 

would become increasingly endetnle during the Fate 
Cretaceous, l^egiiuiing at appro\imal('ly 90 Ma. Tlu 

fables 1-12 reveal a number of notable |)atlerns iti seccmd hypctthesis, fornudaled by our uorkuig gi-oiij) 

(e.g., Krause et ah, 1997b, 1999; Sampson (^t ah. 

the distrd)ulion of Cretaceous Ccaidwanan lerresli-ial 
vertebiates. Tlu^ same (amil) -h.A el taxa of cj-ocodyli- 
lorms. non-avian dinosaurs, and mammals thai were 

1998, 2001) and recently dubbed the "Alrlca-lirsl"^ 
hypothesis b) Sereno et ah (2001), jxisits cosmopol- 

shared among Madagascar, the Indian subcontineiiL itanism of Fate Cretaceous lerrestrial (iondwanan 

Volume 93, Number 2 

Krause et al. 

Late Cretaceous Terrestrial Vertebrates 



120 Ma 






J r 


100 Ma 







80 Ma 




60 Ma 







120 Ma 








100 Ma 


] L 




80 Ma 


] [ 




60 Ma 






Kigurc 8. Scheniallc palt-ogfographii- maps of iiiajnr Condwaiiaii landinassrs rxcliisive of Australia and soiillicrn Kiirope 
at 120, 100, 80, and 60 Ma d('[)ictiMg the major dilTctvnces in pin'porlcd land (-..nnrclions hetAveen llic pan-Gonduana 
hypothesis (left cohnnii) and ihc Africa-rirsl Inpothesis (rii^dit folumn). The pan-r,(.n(h\aiia hypothesis posits separation of 
Sonlli Vmrrica from Africa. South America from Antarctica, and Antarctica from Tndo-Madagascar in a narrow time interval 
](){)_0() \].^^ Xh(> Africa-firsl h\polhcsi.s posits separation of Soudi America from Africa l^efore the beginning of the Late 
Cretaceous, South America from Antarctica in the l^oeene, und Antarctica from hido-Madngasear hite in tlie I.ale Cretaceous. 


Annals of the 

Missouri Botanical Garden 


s t'xtlusivc t)f Aliica. Mure sperilically, llic llu- paltio^rographic reconstruct ioiis prescnicd l)y us 
lallcr model, generally cotisistenl uilli ihe palcogco- c(insist(Mitly show Africa aiul Soutli America still 
gra]ihic reconstruction of Hay el al. (1W9), invoked joined at 120 Ma (Krause et al., 19971): fig. 1, 1999: 
Antareliea (In eonihination \\illi two key land l)ri<lges) fig. 6; Sampson el al, 1998: fig. 4; Krause, 2()():^a: fig. 
as a flispersal rout(> I)(M\V(MN1 Indo-Madagascar (the 2. 1 7; we specifically did iiot use the 120 million year 
Indian snheontlnenl plus Ma(higascar) and South rei:onstruclion in Ilay et al. (1999: figs. 12, lo), \\lu(di 
America following isolation of Africa hy a circum- ilhistrales full separation between South America and 

Africa at this lime, bul inslead employed a recon- 
struction generaled from the wcl:)site ojieralcd 1)\ the 

African sc^away prior to the begiiming of the Late 

Cretaceous. According lo this model, terrestrial 

verlebrate famias on Ahiea ar(^ |)r(Mlictcd to have Hay el ah working gron[) (<htt[)://www.odsn.d(Vodsn/ 

become j)rogressively more ])ro\ineial during the bate services/[)aleomap/pa]eomap.hlml>), which shows 

Crelac(M)us (after separation between South Auieriea these landmasses still conuecled bv a narrow sub- 


and A(j-ica i)rior lo the end of the Earl) Caaac(M)iis). aerial passage^ al 120 Ma). In any case, the porlra}'al 
while those on other (/ondwanati lau(hnass(\ 

s w - 

1)) Sereno ct al. (2004) of our Africa-first hypolhesis 
maiued rclati\ely cosmopolitan until considerably as requiring isolation of Africa as early as 1 dO Ma is 

later in the period. 

Scrtaio el aL (2001; see also Mahha", 2007)) recenUv 


1 tl 

Second. Sereno et ah (2001; b'?28-i:529) concluded 

rei>orte(l tde nnporlaut (Useovery o 

( a number of dial 

. L 

a permanent equatorial seaway of significant 

d(diniti\c abehsauroid iheropods (ab(disaurids and depth between South America and Ab-ica was in |)laee 
noasauritls) in A[)tian-Albiau sliata of [Nig(>r (apj)rox- no earlier than the end of the Albiau," and that "traus- 
imately I 10 Ma) and Ceuomaniau detxtsits of bolli 




antic nitei'chauge may have been operative as laU 

N i g(-' 1- 


and Moi-occo (appioximalely 9o Ma), thus as 95 Myr ago/' Elsewhere in lh(^ same paper, Sereno 

et al. (2001: 1328) stated duil "well-constrained 

i<ling the first con(dusive evidence for the 

presence ol this tdade In Afiica. dliese finils support 
the ])r(;-Lat(^ Cr(*laceons origin of \b(disaur(tidea on 

geological evidence (Reym(Mil & Dingle, 1987; Pitman 
et ah, 1993; Maisey, 2000) ])inpoinls llu^ final 

Condwana, as previously indicatcMJ by several earlier se|)arali(>n of Soutli America and Africa in the latest 
discoveries in Argentina (Coria i.K' Salgado, 1998): Albian (ca. 100 Myr ago), significantly lat(n- than 
Lamanna et ah, 2002; Kaulml el ah, 200;5). Thus, one proposed by the "Africa-first" model (c a. 110- 

alternati\e h\ pothesis of Sampson el al. (1998: 
1050) — that "aludisain-ids originated souietime in 


1^ n 

120 Myr ago)." To chirify, the three pa|)ers cited by 
Sereno et al. do not make such definitive assessments. 

the Early Cretac(MJUs alUa" the t(H'tonic Isolation of Ueynient and Dingh^ (1987: 99) stated thai "final 

Alru-a'' — IS clearly j-ehued. Based [)riinarily on the contiruaital sejiaration was /jro/x//;/}- completed in hale 

new African abtdisain'olds, Sereno et al. (2001) [nol latest] Albian time" (emphasis and bracketed 

concluded that the evidcaice therefore supj)orts tin; W7)rds added), Pitman et al. (1993: 23) stated that "the 

pan-Condwana hypothesis. We disagrcfMvith ihe latter j)oint in time of final separation must be l).Mwe<ai 

contention, and regard the Africa-fir>t hvp(. thesis to 84 Ma ... and 106 Ma." and Maisey (2000: 28>5) 

be more consistent with iIk^ available, although 
admitledl) limited, evidence (sec b(dou). 

concluded that a permanent equatorial seawav ioiuing 
the South Atlantic and the western Tetlivs Ocean had 
developed by I he late Aptian (which etids at 

address several statements by Screnr> et al. (2001). a|)pro\imately 112 Ma; Grad.-,Lciu et ah. 2001). That 

First, these authors (daimed that ihe oriiiiual forrnu- 


ore assessing tins issue, il is neeessarv to 

said, it should l)e pointed oiil that there is othei- \\(dl- 

lalion o( the Alriea-firsl hypolhesis by Sain])son et al. constrained geological (w idence (NLirnberg & Miillcr, 

(1998) included the slipLdatiou that Africa and South 1991: PlcLsch et ah, 2001) for a ])crmanenl marine 

America were hdly se[)arati'd by 1 10-120 Ma. eonneetion between the central and southern parts of 

Speeifically, Senaio et al. (200 1: 1328) statcti that the Atlanlic Ocean, separating South America from 

the Ali-ica-first modtd. as portrayed bv Sampson el al. Africa by the late Aptian-early Albian. ap|)ro\imat(dy 

(1998), "Miows a circuui-African seaway in the Early I 18-10(> Ma (Cradstein et ah. 2004). Again, we have 
(■r<^taceons (ca. 110-120 M)i- ago) lliat isolaitnl the 
conlinenl from othei Condwanan land masses." 

Whereas Sam|)son et al. (1998: 10.50) did state thai (auTcut gxM.physical and paleogeogra])hi 
"'South Amciica separated IVom Africa befor(^ 

100 xMa'' and, in llu^ caption lor Elgure 4, specified As su(dK ihe jirimary distinction concciiiing this j>oiiit 

never argued for separation of Ab-ica and South 
America as early as 140 Ma, bul il mnsi be noted thai 


c (wuienee is 
suggestive of sepaialion before tlu^ i'Wil of the Albian. 

"circa 120 Ma," (dainrs for se[)aration as earl) as is that Sereno's foi-mulation of the juui-iioudwana 
140 Ma were not made in that |)ap<M-, <tr in any oilier hyjxtthesis views separation betw(MMi South America 
paper- ])id)lished by our working grouj). buh^'d, all of ai^d Africa as having oiuau-red after llu 

■ (MH 

I of I 

Volume 93, Number 2 

Krause et al. 

Late Cretaceous Terrestrial Vertebrates 


Early Crelaceous, whereas the Africa-first hypothesis boundary, but the persistence of land bridges that 
supports separation before the end of the Early permitted fauna! exchange through Antarctica be- 


tween South Anierica to the west and Indo-Madagas- 

the "Africa-first" model." While we asree that this 

Third, Sereno et al. (2004: 1328) made the claim car to the east until well into the Late Cretaceous. 

that ''other faunal evidence (notosuchian crocodylo- According to this view, early stocks of abelisaurids 

morphs (Buckley et al., 2000) and gondwanatherian (and other vertebrates) were present on at least South 

mammals (Sampson et ah, 1998)) no longer supports America and Africa (and perhaps other Gondwanan 

landmasses) by die late Early Cretaceous. Rifting of 
evidence is far fi-om strong or highly resolved, Sereno South America and Africa toward the end ol the Early 
et al/s conclusion simply does not follow from Cretaceous isolcited at least two stocks of abelisaurids, 
their explanatory statement that "Ahican crocodylo- one on each continent. Currently, there is no reason to 
morphs of mid-Cretaceous age (Aptian-Albian) are assume that they had spread into Gondwanan land- 
most (dosely related to taxa of comparable age on masses outside of Africa and South America at that 

South America (Buffetaut & Taquet 1977, 1979; early stage, although this scenario is not inconsistent 
Sereno et ah, 2003), and the absence of gondwa- with avai]al)le evidence. Similarly, in the absence of 

^fleets only the non-existent record of fossil evidence, we cannot yet know what happened to 

natheres re 

the isolated stock of abelisaui^ids on Africa during the 
Late Cretaceous. However, on the rest of Condwana, 

mammals on Africa during most of the Cretaceous." 
Close relationships among African and South Amer- 
ican crocodylomorphs of Aptian-Albian age, which we a basal stock of Cenomanian al:)elisaurids (of which 
do not dispute, cannot serve as evidence for no longer there is evidence in Argentina: Eamanna et ah, 2002) 
supporting the hypothesis that Africa was the first diversified into closely related forms obser\^ed later in 
major Gonciwanan landmass to become isolated. the Cretaceous in Argentina, Madagascar, and the 

Indian subcontinent. Lacking fossil evidence, this 

Furthermore, the recent cladistic biogeographic 

analysis by Turner (2004b), reviewed above, demon- hypothesis does not stipulate when during the Late 
strated that crocodyfiform evidence is indeed consis- Cretaceous those basal stocks (or their descendants) 
tent with die Africa-first hypofiiesis. Finally, the first arrived on Madagascar and the bidian sub- 
presence of sudamericid gondwanatheres in tlie continent; that is, they may have been present at the 
Campanian/Maastrichtian of South America, Mada- time South America and Africa separated or they may 
gascar, and India was primarily used to sui)i)ort the have dispersed much later from South America, 
hypothesis that this enigmatic clade of mammals was Flowever, this view is consistent with uU phyh)genetic 
much more cosmopolitan in its distribution in the evidence presented to date (Sampson et ah, 1998; 
latest Cretaceous than previously realized (Krause et Carrano et ah, 2002; Coria et ah, 2002; Wilson et ah, 
ah, 1997b). The absence of sudamericid gondwa- 2003; Sereno et ah, 2004) and posits that the derived 
natheres from the Cretaceous of mainland Africa abelisaurids (including several horned forms) present 
(which, in fact, may not f)e the case — see Krause et in the Maastrichtian of India and Madagascar on 
al., 2003b) is no less supportive of an Africa-first tlie one hand, and the Campanian-Maastrichtian of 

hypothesis than it was when the paper by Krause et al. 
(1997b) was }>ublished. 

South America on the other, shared a more recent 
common ancestor than either did with abelisaurids 

In light of the discussion above, let us reexamine from Alrica. 



current evidence and assess the claims and 

Concerning [)aleogeographic reconstructions, none, 

implications of the competing biogeographic hypoth- including Scotese (2001), depicted a situation in 

which all three land briflges were severed at 

eses by focusing on established geologic and biologic 
constraints. First, die pan-Condwana hypothesis, as 
defined f)y Sereno et ah (2004), posits the existence of Cretaceous, a[)proximateIy 100-90 Ma. As reviewed 

approximately the same time in tlie early Late 

above, current evidence suggests that the South 

three narrow, intermittent land bridges, all severed in 

the early Late Cretaceous, approximately 100-90 Ma: America/ Africa land bridge ceased to exist prior to 

one between Africa and South America, another the Albian/Cenomanian boundary (i.e., prior to 

between South America and Antarctica, and a third 100 Ma). Indeed, even Scotese (2001) depicted the 

between Antarctica and Indo-Madagascar. Geologic two continents to be already well separated ])y 94 Ma 

evidence in support of tins model ^vas based on the (Schettino & Scotese (2000) show separation at 

paleocoastline maps of Scotese (2001). In contrast, 

100 Ma). Current geologic evidence is most consistent 

a revised Africa-first model, incorporating recent data with the separation of Africa and South America (and 

on Afiican abelisauroids from the Albian and thus the isolation of Africa) by 100 Ma (Lawver et aL, 

Cenomanian, postulates die separation of South 1992; Smith et ah. 1994; Marks & Tikku, 2001; 

America and Africa prior to the Early/Late Cretaceous Scotese, 2001; Kent et ah, 2002). By contrast, a land 


Annals of the 

Missouri Botanical Garden 

South Anicrica and Aiilart-tica is I he paii-Coiiilwanaii h)|)(}lhesis of Sereiio et a1 

hrid^i' hchvceti 

thought It) ha\e been present ihtoii^uiionl tlie Lale (200 1). 

(j-elaceous and nnlil al h^asl llic earl) I^ocenc (ha\v\er 

I' inally, I he mete presence of alndisaunds an( 

et ah, 1992; Woodlxirne & Case, 1996: I hiy el al., noasanrlds on Africa 2,"^ or more million years [>ii(ir lo 
1999; liegnrro el al., 2002; l,awv(M- & Caha<^an, Uieir oe(an-r(^nce in Madagascar and Tnilia diK^s n(»l 

conslilntc c\'idcncc rclulini^ Hie Ali'ica-firsI h\podic- 
sis. AJdioudi reecMit discoveries demonstrate the 

2()();5); there is no evidence lor a tej-mi nation of 

coinicctioii 100—90 Ma. Fin: 

ill\'. as ( 




the limit 1^1!, of separation ol Antarctica from Tndo- presetu:c o( ahclisanrolds in the Eai'lv Cri'laceons 

M : 

i<ht^uascar is eonlroversial. Most rccoii^trnctions and earliest Lal<^ Cretaceons of inainhmd Africa 

indicate ihat Indo-Madagascar liccatnc Isolat 

1 f 

CO iroiu 

eertanily an nitcrcstin^ and signilicant imonii' 


f i n d i 

all other (iondwanan landmasses about 120 Ma. sonu^ phxiogencllc analysis does not include placement of 

50 million y(\u-s prior to th(^ lime that the Mae\arano the recovi^'cd foiins a]]ion<2; the more derived mcni])tas 

vertebrate assemblage (as \\(dl as tliose from bidia) of this clade (Sci-eno et ab, 2004). bid<'cd. the 

was dc[)osil(Ml {e.g., Lawver et ab, 1992; Smith <M ab, abelisanrid A*//^'-o/),s- is postulated by Serene et ab 

1991; Marks ,K' TIkku, 2001; Rotstcin cL ab, 2001; (2004) as iIh^ basalmosi member of the gionp. Thus, 

Scotese, 2001: Kent el ab, 2002; l>(a-uard cl ab, 2(){)o). although it appears that Abica did nol separate from 

Notably, and in stark contrast, houcver, ihe Ice-tonic South Ann'rica until near the Earlv/bale Crelacciais 

pi'o\ ides suppoi'l (or the boundary, the closest relatives of Majinigdlholiis and 



Hi!" o 


IV e 

t ab 

sc(Miario jxisitcd l)\ the Ab-ica-brsl li)polliesis in ihat 
a land bridge between Antai'cllca and Indo-Madai^as- 

Masiakdsaiiriis from the ^blastrichtian of Madagascar 

are still htund in (^atupaiiian/Maastricbtian horizons of 
car was mainlalned iinlil apj)ro\imat<dy 80 Ma (cb South America ;md India. As such, there c\i>ts no 
Case, 2002). Tn neither case is there evidence to fauuLil t^\idcucc to rcbite the hvpothesis that Africa 
iiuHcate s\ iichroneity with the separation of Soutli ^^'^i^ the first among major (Jondwanan laiidmass(\^ to 
America from tather Africa or Anlaiclica at 100- be fidl\ isolated and. perha|is most imporlaiitiv, that 
90 Ma. as poslidated b\ Sereno (4 al.'s (2(l()l) pan- the l(a-i-estrial \crlcbrales of (/ondwanan faunas 

outside ol Africa were shared mitil late in the bale 


In smimiar), we regard the growing \\ciglit of latest 

Condwana mocbd. 

Concern Mtg fauna) e\ ideiR-e 

, III 

e crocodybforms, 

nona\ iau (buosaurs, and manmials rcco\<a'cd from the 

Macvarano fOiniation of norlhwestcrii Madagascar are Cretaceou> biogeogiaphic data a.> evidence iii sup[)ort 

taxononucallv most similar to tlios(^ known from '^' ^i modified Africa-fnst hvpothesis. The (dose 

Campanian/Maastntditiaii liorl/oiis of South America ndationships of teirestiial \ertcbrales that li\cd on 

and the Indian subcoiit incut (f\ranse el ab, 1997b; the bidian subcoiititUMit and Madagascar near tluMMid 

Hucklcy & 13roclui, 1999; i]uckle_\ el ab. 2000: 

Krause, 2001; Wilson el ab, 2001: Currv Kon^rs. 

(tf the (a-ctaceous to p<aiecontemporaneou-^ la\a in 
South Atnenea appear iucomjiat ibie \\[\\\ an\ pro- 

2002; Prasad ^ di^ ba|)parent de \]i\n\\, 2002: Turner, l>osed lengthy separation o[ lUdo-ivuKiagascar an( 

f Iiido-Madairasc: 


2001b). Ri;caus{i .streni^th of biog-coi^ratthic sii^nal is South .\inerica prioi- to the Maastri^dilian. whctlua' 

thai duratiftn was approximately SO million \ears. as 

[troportnitial to the nmnber of j)li) logeiicticall\ in- 
dcjxaidcnl groups possessing the same eongiuent 

indicated b) mosl i-eccnl paleogeographic rcconstiuc- 

patl<M-n of area (dadograms. it is significant to note that tions of Crelac<'oiis Combvana. or appro\im;ilely 2S 

million y{^ars, as posited l»y the pan-C{ tnd wana 

I he palUaiis of similarit) are repeated anumg a grow lug '^^d 
nniubei' of [)hylogenetical]\ iudcpendcMl groups (e.g.. hy|)othcsis. 
notosiichids. peirosaurid>. tretnalocliam])sids. and the 

unclassifu'd nu'tasucbian genus Arai'ijn'sin 

crococb b forms; abebsaurids. noasaurids. and salt- 

Jnis amttiig 

1 -IleriUiiri' ( iiu-d 

asauriiics among nona\ ian dinosaur^; and sudamer- 
icids aiiKnig mammals). This pro\ idc.> exidence for 

giUliji gen. el .^p. 

a biiih d 



(iegr(H^ oi cosmo[)ol ilamsni anuMig latest 
Cretaceous Condwanan faunas outside of Africa tliat 
was not fully apprcciaUMl [)rior to rccov^M-y ol' the 
Mae\arano ass(MnbIage and is unprcdicted basc^l on 
mosl rci-cnt paleogcMigraphic reconsli'iief ions of the 
soul hern supeT-conlineiit (e.g., bauM-r el ab. 1992; 
Smith el ab, 1991; Scotese, ]99r>. 2001; Marks & 
d'ikku. 2001: Rotstcin el ab. 2001: Kent et ak. 2002: 
Hernard et ab, 200.5; Schettiuo X Scol{>c. 2005) or 

Ap<'stigiiia. S. 2(H) 1. /JonildSduni salgiuloi 

tit)\ .: \ l)r;ike(l sjiifopod Ironi die I,ate ( !i"f ■hiccniis of 

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Averiaiiov, A. (),. J. D. Arcliihaid .^ T. Maiiin. 200.3. 

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Based on llie iin(H|iial(Hl soiitlirrn Kate Crola('(M)iis-(^riK)Z(>ic record, the history of South American land niainmals is 
divisiljJe itiL(j Iwo inajor ej>l^()d(^s we term the (/oriduanaii l^iilsode and ihe South Ainericau Episode. The for!U(M- episode is 
dislinguish(Ml by die iiorllieiri and central Pata^onian Argentinian record, while the latter is niostl) leased on the exlra- 
Palagonian Argentinian record. Hie Condwanati I'^jji^^ode is so termed because it is exclusively represented b}' endeniic 

matTitTials of Condwanan origin, i.e., Mfvsozoie hneages. In contrast, the South American Episode is almost exclusl\(d\- 

distniguislicd hv endemic Therian mammals \\lif>se ane(;stors emigrated from the Eaurasian INOrlli American Continent. 

Tlicsc lw"o major, successive, and for some lime supcrim[>osed e])isodes are tlie result of the geologic luslorv of llu; South 
American Phite. (1) This phile was par! of th(' Condwana Su|)crconlinenl until about 120 millions of years before Picscnl 
(niybP), when il began to se|)arale and (hifled westward (but al\\a\s south and lelalively near the North American Plate). Unlil 
about 'M) myhP it was eonnecled ht Western Arilai-ctiea, and through it to tnosi of die Eastern Gondwanan conlincnis. (2) By 
approxlinalely 125 iiiybP, Domielly"s "Elood Pasall" was Initialed. After its cessation by 85 myl}P a variety of compressive 
tectonic hvUni'es around the C^aribbean Ix'gan, i.e,, subthaiion and island arcs or continental margin magmatism. Tiiese 

features probably permitted ihe first known inIer-Am<-rican exchangr (>( tetrapods, dinosaurs sucli as Hadrosauriflae from the 
rising North American continent and TItanosaurldac Saltasaurlnac from the South American continent. Probably bv the lalesi 
Cretaceous iliese geologic fcaLures also ptainiltcd the Immigralion of the first blu^rian, which gave rise to the native South 
American land mammals. (3) The g(M)logic dcbnltion ni soulliern ('eutral America is the last and nu>st inijiortant phenttmenon 
relal(Ml t(t the final connection of both Americas. Ry 12 mybP the sultmarine coiniection of Cenli'al America with South 
America began, and sul)se(jueiit v(tlcanic island aics permitted the beginning of The Great AnKTiean Biotic hitcrcliang(\ 

According to the Palagonian recortl, the abs(Mice of Iribosphcnlc mammals and the total extinction of the endemic uon- and 
i:)re-li"ibosphenic mammals are the most outstanding e\(Mits cliaracterizing the Cond\\anan Episode. Up to the bt.^giuning of the 
South American l\pistKle (i^ar'ly Paleocene), lew Gondwanan lltuuiges of matumals (a native Gondwanadieria and an enrlemic 
Dnolestoid) sur\i\cd in the South AiTicrican conllnent: auolher related Gondwanatheria taxon survived u]) to the Eate Eocene 
in Westei-n Antarctica. Ihese Gondwanan survivors lived logether with die first, but ad\anced. inmiigrant Ihcrian that 
initiated the South American Episoilc. Allhougli not conclusiv(*ly dt^monsti'atcd, there are some suggest htns thai this 
superj)osilion began (\u-lifM-, [irobably by the pre-Canipanian Cretaceous. The hislor)' of endemic Therian mammals 
characterizing the Soulh American l''pisodc began to be known In 1948 thanks to the efforts of the Aniegliinos and (7. G. 
Simpson. These represented the oidy kno\vn higher taxa imtl! 10o.5 when Rotiaparle recorded the first non-therian Gondwanan 
lineages in Eate Cretaceous (Cauipanian) ralagonlan beds. Suecessi\c author^ contributed to this hislor), ratilving Sim[)son"s 
statement that the Soiitli American Ceno/oic mammal evolution was episodic. Thus, llic most charactei'istic geobiotlc featiu'es 
of the two major (episodes are based almosi cxebist\riy on the most eloquent Cam])anian-Quatcrnarv Argentinian record. 

Kcyiiords: South America, land mammals. e\obition. geograpliv. Gondwanan Episod(\ South American Episode. 


De acuerdo a registros sin iguales del Crelacico-Ctaio/.oico lardfo meridional, la historia de los mannTeios tcrrcslres 

suranuM'ieanos se i>uede di\idir en dos episodios Importanlcs que llamamos el E[)isodio de Gond\\ana y el Ejilsodio 
Suramericano. I'd primer <'|)IsodIo se distingue per o! regislro argentino patagom'eo del norle y centro. mientias que (d segundo 
se basa sobre lt>tlo en v] regi.slro extra argentino patagtMiico. El Episodio de Goudwana es asf Uamado porque esta I'epresentado 

' 1 extend special thanks to Petta- Ba\en foi- his in\itation to be one of tlu' sj)eak(M-s of (his symt^osium. To be selected among 
such pronn"nent scientists is a gi'cat honor, especi;dl\ l»y so distinguished an luvestigalor as the [director of the well-known 
Missouri Botanical (warden. I \v(»uld bke to ad(h"ess a very sj)ecial acknowlcdgmeni to Alan Graham, as well as lo Mick 
Richai"ds(.)n and \'ietoria llollowclb whose assistance was not onlv uncommon but also decisive in makin*! our stay a r(^al 
pleasure. Without exception, we are also Indebted to all the organizers of this pleasant and successful s}niposIuni. Special 
thanks to Olga M. Monliel. Most of tlie figures weix- maslerfully designed by Aguslln \'inas; others by Eaura Zainpatli, Carlos 
Vildoso Morah^s, and Maretda Tomco. As always, Laura /ampalli conlril)Uled lo \\\c composition of the pa|)er, suggesting 
invaluable syntaclic Ideas. Constructive ciiliclsms and su'i'i;i^slions were made l)v the referees, Richar<l Cifelli and (TuilliM'ino 

Rougier. as wcdl by Vicl()ria C. lh)]low(dl (Srlentlflc iMlilor) and So[>hia R. Balcomb (editor); all LJudr suggestions and 
corrections, without any (juesllon, impro\cd this pa|)cr. It is obvious that English is not my native language. Hence, i leTl (|uile 
a job lor my li-ienf! R. Cifelli and tlie edltttrs!! To all of them, T am very gratefuL 

~ De]jarlaniento Paleontologi'a Vert<-brados, Miiseo de I-a Plata, Paseo del Ros(]ue s/n, 1900 La Plata, Argentina. 

\^N. MissouKi BoT. Gaud. 93: 209-230. Purfjshed on 23 August 2006. 


Annals of the 

Missouri Botanical Garden 

cxclnsi\ar]if[ilr poi- los riKunifrros <-n(lrmi{.!U8 lie (nigon *i;inuK\riiii('(). i.e.. linajcs inosozijicus. Kn (■(witiastc. r[ l-.pisodio 

SuraiiH'ficarKi se (Hslinj^uo casi L\L'lusi\anu'til(' 
laurasift) iKdlcaiiiciitiaiU). 

[tor inaiiiik'iDS trnos (MuleniiLus (_-u}u.s ai]le|<]()s cmi^iaion ( 


It'l roiitiiiciik 

Eslos (los <'[)is()(li()s iin|Kn1:niU's, sucesi\()s v pnr firrto licnipn snlnr|)ursl(>s son el icsullailo dc hi liistoria ji;r()l(')i;ica i]c la 
placa siiiaincric-ana. (1) K.sla ])la('a fortiiaba parte del supei'coiitinenle de rroiiduana liasta eerca de 120 iiiaap. euaridu 
coiiien/o a sc[) y de^[»Ia/aI^(■ liacia (d ocslc (pero sieiiipre al Mir ) rtdalix aiin'iite eerca de la plaea norteanieiieana). 1 lasla 
haci^ eerea de 'M) maa]) esluxo e(nieelada a AiiLirliea oeeideiital, y a lia\'es dc esla a la ina)()i"fa de l(^s eorilineiites 
getidwanieos orietilah^s. (2) Alrrdfiltir de 12.1 iiiaap. empe/i'i la "iiuiii<laeitMi liasallira" ilc Doiitudly. Despiies de sit eesai-i(')n 
haee 8fi inaap, eomenzo una var'iedad de eaiaelen'stieas leelonieas eonipresuas alrededer del {'.arihe, i.(\, areos de islas y 
subdueeioii e Mia^niallsine niariiinal eoiilineiital. Eslas earaeleiLsheas piohahlciiiriilf peiiiiiliereii el piuner inlereaiiilno intcr- 
aiiien'eaiu) eiiiUKitlu de lelrapod(j.s, dinosaiirie^ tales eomu l]a(lr()>aMridae del eoiiliiuMile norteaiiieilcano eii le\anlainieiilo ) 
Titanosaiiridae Salta>aiii"inae d(d eotiiiiiente siiraiTierieano. Pi^ohaMenieiite liaeia fines del (^reiaeitt) estas eararterfstieas 
geologieas latnhit'n perniitierDii la migraeion <Jel jin'nier terio, que dio origer] i\ les mairii'feros terreslres suramei'ieanos. (l]} La 
delinieioii geolTigiea <]el sur de Ainetiea (Central es el I'lltinu) \ ni;'is inifjoilante f<*[i(Miien(t i"(daei(>nado eon la eonexiim liiial de 
anibas Ainrrieas. TTaee 12 inaat» i'(inien/6 la eetiexion suhttiarina de Atiiei'iea (Central \ del Sur, v sul)S(H*iuMites arees de isia 
voleaniees peiiititiefoji el iiiieio del Gran iiilereainhio Bioliee Ainerleano. 

Segini el I'egistr'o patagniiieo. la aiiseiieia de inniiineros Iriliosh'Miieos v la exliiieion total de los inanifferos endT'tnieos no- n' 
pie-trihosfenieos son los aeont('<'iiiin"iilo.s mas exeepeiuiiales i\[\r [aiaelerizati ol l\[)isodio de Coiidwaiia, I Fasta prinei[)io del 
Ejnsodio .Siit:irMei-ieano (PaleocH:n<' lernpfano), poeos linajes goiu[\\;inie()s de inaini'fefos (un (^ondvvanaleilo nalI\o y un 
r)r}*)lestoId<' endeinieo) soln-e\ i\ iei'on en el coiit itieiite siiramericano; otfo la\on ( iondwaiialerio relaelotiado sol)i-e\ i\ i(') liasla 
(d Koeeno I.-wdfo en Antar'liea (H'eid(Mital. ]\slos sohrevivientes de Condwana vivieron jnntns eon el jininer, pero a\ an/ado. 
inmigranlr trrio que iniei('> <d F[nso(lio Suianici irano. Aun(|iif' tio se ha drin()stiado eu forma eoneluvenle, hav algunas 


ias (I 

e (]ue esla su[)eip(i>ieir)n eomen/f') ariles. prol>;d)lcirnMilt^ per el (aetaeieo {)re-Canipauiano. La Inshjria de los 
uianuleros lerios endemii,(» (jue earaeterl/ait el l'>[jisodio Suiamciirano se eni|)e/(j a e()noeet'en lOl^graeias a los e^luer/os de 
los Ameghinos y (?. C Simpson. Lstos nq)r<*seulal)an los uuie(is laxones a\"au/ados eonoeidos hnsia 1985 ruando noi]aj)arte 
i'egistr(') los [irinuM'os linajes ni> lerios de (iou<l\v;iua en deprisilus palagonieos drl (j-elaeieo tar(h'o ((^anipauiarn)). Anioi'es 
[loslerioies eont r d)u> erou a esla hisloria, ralilieando las aliirtiaeiones de Simpson (|ue la e\(iluei(Mi dc lo.-, manii'feros 

sLnamoIeanos i.-enu/oieos fue episodiea. Asf, las earaeleri'slie<is geohiolieas mas dishnliv a^ ile los do.s episodios mas 
importautes se hasan casi e\elusi\ ameute eu el mas (doeuenle registro aigeuliuo del Cauipaniano-C'uaternario. 

iM'noni'cnoN wn i\h:TinM)s 

The liislury rif South Anieri<'an niciiiiiiKds is 

ldv(; Iwo hi^l()ri(*s In one. W ilhin (he 


The puipose of tins paj>ej" is to arialy/<' the firsl 


k (t( i)1al 

unewoi'tv (U piau^ teeloiiies, varying paieogeog 






geologic-geographie plKUioiiieiia 

related (dlniallc-(^n\ ii'onrTiental changes, that iiov- 
enied the 

e\()lutionary history of land nianunals 

led [(I date m fl 

I Pal 

reeoriied to dale m me pi"("sem raiagonian regain o 

iho South Anieriran eoutiniMiL This is not a nieix 

and the stales divided llie history ol land inaninials recorded 

in the southern South Anieriean i-ontineiil Into two 

distinct episodes: the Gondwanan Kpisod(^ and the 

f South AnuMiean Rpisode. In lacL die Irihospheiiic 

Late Jurassic l)eds of the 



s leeoK e< 



anal \ sis of ll 

le s\slenialie eliaiigcs 

Lhat ; 

sLiei-essi\ el\ 


occurred ni ihe niauuua 

eomuiuuities during the 

e.orres[)ond lo two sonic what distinct geograt)hical 
situalions when South Ainci'Iea was an emerging 

pr(~scnl South Auicricaii continenl (Fig. 2). as W(dl 
as ail ad\'anccd pretril)osplieiuc nianiiiial recorded in 
s,hort titue that South America was an island coiili- Early Cretaceous beds (Fig. 3), ];olh in Patagonia, 
neni (a slioit tune because, accoi'dmg to /a<'hos et al. 
(2001 ), tin; island eonlincnl Ijcgan to be ti)tally 
isolalcd from ca. .'U) nivbP (Fig. 1), nol from the coiititient slid not well separated from the Aliiean 
beginning of the Cenozoic as Simpson (e.g., 1980) and continent. Thus, ihe rrondwanan and South Xnaaican 
followers dioiight). While the history f;f South Fpisodcs are' llie (Uily two [>rcsenll_\ well-t;slablished 
American land mammals has \)cru (^xlensively major episodes in the history of Soudi American 
treated, virlually all ^^uell Irealunails were published mammals. Widi ihal in miiuK 1 will nol detail die 

hefoi'e recognili(Mi of ihe reeentl\' (lisco\ered Gond- 



1 features of the sucx^esslve mammal 

wanan uuumnals (Campanlan and the la^t earliest communities as, for exanq)Ie, was done following die 

Paleocerie rt^presentalives). Thus, ihis paper empha- pnndously reeogni/tul launislie cycles (Pa.-^cual et aL. 

sizes the dislinci history of ihc Condwanan mammal 1996). For example, widiin tlu^ Soiidi American 

comuumilies vvilli resp<M-| lo (he r(dati\(d\ w(dl-knmvn Fpisode 1 will onlv j>oint out die maui i-\('nts iJiat 

Cenozoic and Rfvenl South AnKM'ican mamtnal (diaraclerize what Stehli atid Wtdil") (lOH.^) distin- 


gui^herl as Tln' CreaL Anu-jiean 

Hiotic lutcrehange. 

Volume 93, Number 2 


South American Land Mammals 


Figure 1. The geogi;i|tlii(' silitalion of South America and Antaretiea 30 niyhP. According lo Ziichos et ah (; 

, ihe.^ 


continents were totally sepai'ated hy lliis lime, thus heginning ihe transcendenLal isolation of the Soulli Aiiieiican conlineut. 
Land masses 30 nubF are oulliucd in bhick. 

which has been a|)ll\ (.Ievel()[)etl by \\ el)b (2006 tliis 

The hierarchical arrangeiiUMii of the SALALVs 

issue) and, inrlepeiulenlly, but eomplernenlarily, by reveals ckisters lliat represent evolutionary episodes 

Coates (2003). 

of maninial eoniniunilies, not onl) taxonoinieall) , bul, 

As Sunpson (IQ.IO, I9{i()) correctly indicaled, the more iniportanlly, according to ecological niodifica- 

hislory of South American mammals was episodic and tions. Orliz-Jaurcgnizar (1986) performed a multivari- 

divisible into sigfuficant intervals of comj)ositioual ate analysis of similarity among SAbMAs, a method 

changes, and thus provides the biochronological that was subsequently revisited and updated l)y 

framework in which to understand their evolution and Pascual & Ortlz-Jaureguizar (1990) and Pascual el 

the evolution of iheir mu ironments. Because of this, al. (1996). As Ortiz-Jaureguizar (1986) did, these 

most North and South American paleomanmialogists latter authors used SALMAs as o|)erational laxonomic 

use the Land Mammal Age (LMA) — in our case, the units ((TrUs) and families of tlie Lale Cretaceous and 

Soulli American Land Mammal Age (S/VLMA) — as the Cenozoic Land-Mammal Ages as "cliaracters." Tliey 

basic biochronological unit (hut see Clone & Totmi, were able to recognize four hierarchical ranks of 

1995). "Mammal Ages were intended to represent SALMA organization, distinguished as Faunistic 

(hvisions of the Cenozoic, based on characteristic Units; from lower to higher tliese were Faunistic 

groups of fossil mammals whose temporal relationships Subcycles, Faunistic Cycles, Faunistic Supercyles, 

and Faunistic Megacycles (Tal)l(^ 1). Major changes 

indicative of a particidar interval of geologic time... observed among mammal comnunnties (Pascual & 

att(Mition was given to first and last occurrences, 'iiidex Ortiz-Jauieguizar, 1990; Pascual ct ah, 1996; Pascual, 

fossils' were noted, and characterizing assemblages 2001) appear lo be concomitantly related to major 

and overall stage of evolution were thought to !)e 

were listed'' (Wood])urrie, 1987: 1). 

environmental changes, apparently correlated with 


Annals of the 

Missouri Botanical Garden 

Canad6n Asfalto Fn 
{Asfaftomylus patagonicus) 

Estancia Laguna Manantiales 
{Ameghinichnus patagonicus) 




■'^ 2. The palr'og(Migra[)hic silitalmn ol llir Soulli Aiiiciicaii (.■ontiiiciit h> ihc vikI i>l ihe JLlra^sI^:', 155 rii)l)l\ i.e., >li[l 
fonnrclcd [o tlir rrnuiiiiiii^ C'.nnrhvanan contiiienls (Jhle Sniilli ct al., IWlj. This a|i|>arenlK' explains the jM-rsistcnrr of 
Eulhrriaii tnanimals In what was going In he ihe Patagoiiian trtiiloiA . and ihrii al)sen(.:e ihning ihr l*alagonian Lair Crelaccons 

Condwarian Episode. Asjulloniyhis pufcf^onicas lianhnU Matlln, Orliz-jaurcguizar tX I^ncrta. 2()()lZ Is a Ealc Jurassit! 
tt Ihosplicnic nianinial foutid in Palaguiila (ChLilnit), and Aini-L!:!iinic}iniis jxiiaiionicus Casaniiqiicla. 1961 is a l.alr Jniassic 
i<-hrnta o( a snj)])r)S(Hl Pantothoria. also (loin I'atagonia (Sanla (aiiz). (in^\ shatHng i-cprescnls land masses 1.5.5ni}l)P. 
(MtKlKied (roni Sniilli el a!.. 1991; reprinted wllh llie permission of ( iamhiidge Universllv Piess.) 

worldwide dlastropliic j)li(Mi()niena. We use dia.slropjh- nological (dassifu-ation lo LaU- Cretaeeous inanirnal 
ic pliriiotiu'iia in \[^ eortiprehenslve bcnse coniiiuiiilties from Palagonia known to (hilt^ (SeiJlalo- 
in{dii(ling llie fragnKMilalioii and (IrKling ol contltuMils, 
sea level elianj^e's, etc. \\'e recenl1\ (Pascnal tK' Orli/- 

Yane & Pascnal, 19IJ4, 1985; HonaparU^ et al., 199;5}, 

Ineliuling the rtH*enll\ (liseov(M"e( 





Jain'e'^uizar, P)*)2; Pascnal et al., 1996; l^asiaial & 



ng I^deocene tormalion thai documents ttie lasl 


Or[i/-Jaur<'gni/.ar, in press) also applitnl this hicxdno- known CMinduanan snr\ Ivors. To axoid repclilion, and 

La Amarga Fn 
(Vmcelestes neuquenianus) 


I'igure i^. ITr piniioidial South AuH-riean and Ahiran continents had soinewhat 


diilt(Ml ajiai"! hnl were sti 

eoinieeled h\ \l].^ ni\hP. lhi> e\])lanis \\\\\ tlie Pari\ (a^etacrous \ incclt'^Ws nrit/jucntaiius. reeordi-d ni die nDrliiweslern 
Palagonian Im-iI n[ La Amarga Forinallon. is not part of ihe fhnidwanan Kf^i^ode. C,\v\ shading refMwstaiLs land masses 
L"^)5 ni\hP. (Modified hom Sniilh el ah, 1991; i-<'piinled with the permis^ion of Camhrldge Lnivcrsilv Press.) 




Laiul-inatnnia! Ages: dates. 

rautii>tic Liiiils, and the main ilinuilic and tan ironnicnlal indlcatoi's. 






(»€] (SAVIN etal.,1975) 

t IS 26 







o -— 

u- O 













1 Megafaunal Extinclion 

2 Arrival of mart 

i Climax of thfl Interamfififian tnterchangg 

4 First record "logionaries" of North 

American origin 

5 Cilm^x of hiqh^;rownod "ungulates^" cursorial 
gfgantfc rocknta and large cursorial edentates 

6 Major expansion of soofhern plains 

7 Beginning of Patagonian aridity 

a Last record of Phmalos in high (atttud^s 

3 First omtgraUon (caviomorph rodonts and 
tardigrade adenlates) fo West Indies 

to Balanced woodlands and gra^^^lands 

11 First record of ^'cavtomorph*'' and P^atyrrtiini 

12 Firsl record of auhypsodont "ungulates" 

13 Racord of fossil mammals in Antarctic 
Peninsula indtcatas to warm climates 

14 Climax of PlesEapid-llK^ marsupial 

15 The grasstand cnvlronmonts bogin to be 

16 First record of protohypaodont "ungulates'' 

17 Biogeographrcal dtfToroncoK between lower 
(forested) and higher (op«n) latitude habitats 

18 Increase of the diversity of xanarthran 

21 Unique association of 'northBrners'^ with 
Gondwanan mammals 

22 Record of the first non-AuBtraHan monotreme 
(ornithorhynchid) and last occurrence of 
Condwanan pre-nontrlbo»ph©nfc mammals 
with endemic South Amerkian marsupials 

19 Wam^ to temperate cHmates and 
predominance afforested habitats 

20 Highest diversity of marsupials 

Sea 21 and 22 


23 Only pro- and non-trlbosphenic Gondwanan 


24 No record of mammals 

t ^ M 

^ r n 


























Annals of the 

Missouri Botanical Garden 

I I 

R^s, 1 ncrciii 

American land maminal-ljeariny beds l>iil also for all 
related lidiostiatigrnphiral nnits (Amegliiiio, 1906). 

to provide a synopsis o( ess(aitial (ealu 

sunuiiarize llie main evoluliuiiary evenUs that mark tin 

history of SiHilIi American iiuunmals according to ihe This was his pcclic orig'uiale, which so negali\ely 

higher Faunislic Cycles (Tahle 1), allhough In some inflLUMiced his (otherwise extraordinary work. This 

eases transcendental events puncluale these inelnsive lransc(Midenl error prodneed an ahnost universal 

Faunislic Cycles and $uhc}('les. 


None of the three of ll 

le most outstanding 

reaction against him, especially whvn he suggestively 
named monkey ((aToidea) remains, found in what \\c 
look as early Eociaie heds of Patagonia, Uomimciihis 
paldgonicus Ameghino (Ajneghino, 1891). Ahoul this 
species he wrote ". . . es uii mono de caracLcrcs muy 

comiaisseurs of the South Amtnican extinct and elevados, y lo considero como formando j>arle de la 

extani land mammals, Carlos and Flon^itino Ameghi- h'nea (|ne eondnce al homl)i(^ y a los antropomorfos'' 

nos (sec Simpson, 1948: 19-26) and C. C. Simpson (AuK^ghino, 1891: 291). 

(19P)()), were aware t)f the nu-cfttly Incorporated Soudi Sim])son (1980), in turn, accepted iIk^ Cretaceous 

American Mesozoic mammals. Iltnvever, F. Ameghino age of the mammal-hearijig IJmayo Formation discov- 

ajid Sim[)son, based on distinct, sup])osedly positive, ered by the French paleontologist R. Sige (Grambast 

evidence, did consider ihal they knew them. For et ah, 1967; Sige, 1972) in the southern Peruvian 

example, C. A 



found dinosaur- Hke teetl 


An(h's. Hiese French paleontologists correlated this 

associated with mammals ol Casamayoran age (early formation with ihe marine Vilquechico Formalion, 
Eocene) in central Patagonia (Ameghino, 1906). \\ exposed further to the north and undoublediv 

zvidiodoni teetli as Cretaceous in a<re. and \vron'ilv used the same name 


meghino intcrpreled these 

pertanung to a carnivorous dinosaur (Ameghino, 

The mammals collecled in the Umayo Formation were 
1906). Simpson (1932, 1933, and particularly, later dcmonslrat<Ml to be early I^ih^xene, not 
1937a, 1937b), using relaliv(dy complele, and dKTcr- Cretae(M)us, in age (Crochet, 1979). What Simi)son 
ent, remains, dtMuonstrated that these teeth pertained (1980: 39) express*^! about these Peruvian mannnals 
to a cuiioLis and uni(|ue terrestrial crocodilian species, is quite irrstrucllv(^: ". . . it would have Iun'u expecled 

w ( I u 


occur in 


were inhabitants, at h;ast, dining the Fale Cretaceous 

which he named Scheciis icucorhinus Simpson and that mammals like dicse 

included in a ntnv peculiar infraoider he named Cretaceous of South America." Simpson did not adiiut 

SeluH'osuchia (Simpson, 1937a), In 1 9-16, E. H. that non-tribospluMiie and pre-tribosphenic mammals 

Colbcit accepted Simpson's r(X]uest to finish his study 

and published a mimographic stiuly on the best of the South American continent, and by extension — 

S[)ecimens collecled !)y Simpson and his staff ol" the considering his non-acceptance of the Phite Tectonic 

American Museum (jf Natural History of New York rationale^thal what w^e pR^sently act^q^t as the 

(Colbert, 191-6). Colbert corroborated Ixtfli the croc- Condwana superconiinent had no such |)rc-Cenozoic 




nature of this specimen and that it was mannnals as inhabitants. 

slratigiaphically associated with mannnals of Eocene 

It has lo be remarked that what was k 

nown !))■ 

age (Casamayoran SALiVlA). However, even at the Simps(m (Simj)soii, 1980) as the "curious history" of 

1 remains, he SoiUh American mammals was bas(Ml only on the 

lime lie studied those 



descended from Faurasian mammal immigrants fn)m 
the primordial North American continent. No Cond- 

considered the rclat ionsliips of this new crocothic to endemic Cenozoic mannnals, the majorih of which 
b<^ {[U(vtionablc (Cell)ert, 1916; see also the conclu- 
sions ol Caspailul. 1981). 

()( course Simpson's pa])(M's, and Colbert's coru-lu- Avanan manmial was kjiown until the 1980s, wlu-n 

sive paj)cr, wvvc unknown to F. Ameghino, who died Bonaparte and staff (Bonaparte et al., 1984; Ponaparte 

in 1911 thuiking that suj)posedly carnivorous dinn- & Soria, 1985; Hona|)arle, 1986a, 19861). 1988, 1990, 

saurs lived in South America duriuii the Cretaceous 1996) found the first un.juestionable Eat(^ Cretaceous 


and were associated with more a(l\anc(Hl mammals mannnals, and sinuihaneously Pascual and staff (e.g., 

than w(M-c knouri frf)m anywJu^n^ els(^ in the world. Scillato-Yane v.^ Pascnal, 1981. 1985) found the last 

Conse(iuently, he regarded tlu-se manunaFbearing reliclnal represetUatives, also in Patagonia but in beds 

b(^ds wUh supj)osedly cai-riiverous dinosaur teelh as tif earl) l^ileoccnc age. None of tlic re]ali\c'ly well 

Cretaceous ni ag(% whereas Simpson later cciusidcicd known Ceno/oic and li\ing mannnals show (eatur^^s 

these beds lo be Eocene In age (Simpson, 1937a). indicating a Condwanan anc(^str). 

representing the Casamayoran SALMA (Table 1). The Condwanan mammals completely (hsa[)peared 

riie iransccuding point is that, on this basis, F. by the early Paleocene, at least in Southern Soulh 

Ameglnno built a chronological scale that was too <»ld AuK^-ica, in contrast lo wliat hap])ened. lor examplt\ 

and which he ns(xl as standard not only for South widi tlie Monotrcmata in Australia. Probable Cond- 

r\ 1 

Volume 93, Number 2 


South American Land Mammals 


Los Alamitos region 
[Gondwonafherium patagonicum) 

La Colonia region 
[Reigitherium bunodontum) 

Fi«;ure 4. BclwtH-n 8S and 6'^ mybl' a seaway hisrctf'd the Sdulli Aitiorican continrnl iiilo two paleohi()g(M)grapliic 
provinces {fide \]\t)\u <.K dr la Fiienle, 1993). U is likelv that niosl of lliis inlerval was the eliniax of the Cunduaiian Episode, 
and hv ils end die first Therian iinniigrants from Nortli America inaugnraled die Soiiih Ameilcan Epi.^udc. Los AlaJiiitos region 
and La Colorna re<j,ioti are llie Iwo eoetaiieous Campanian Palai^onian localities where die Iwo indicated (Hmdwanan laxa 

were lo 



waiian survi\al candidates are ihe Xenarthra, despite und()uht(Tlly eulherian mammal, hased on a molaiized 
ihe fad dial none have yel been found in Soulli premolar (//o// mV//',y/^Je Gayet et al., 2001). This may 
AmfMJean LaU^ Crelaeeons or earliest Paleoeene beds. 
Cunstupienlly, Simpson's (Simpson, 1950: 363) 
interprcdalion of what he termed ''episodic hist 


well represent the Aneienl Imnugrants from North 



dial inaiigtn-aled the South American 



F[iisodc. We (jriginally recognized ihose two major 
of Soudi American mammals was correct, but only episodes as stages, plus a third, the Late Pleistocene 
applical)le to \hc Cenozoic mammals of which he was ''Neotropical Stage'' (Pascual, 1996, 1998: Vizcai'no et 

al., 1998: 202). I lowever, herein I recognize those tw^o 




and w(dl distinguishable episodes as 

s Tl 



Condwanan ICpisode and The South American Epi- 



The best current Mesozoic record of South 
American land manunals is almost exclusi\(d) 
Patagonian and Late Cretaceous (Campanian) in age 
(Fig. 4). Comj>ared to the Cenozoic record from the 
entire continent, the Late Crclacaeous evidence 
demonstrates that the entire Soidh American land 


To date, the Condwanan Episode is l)est represent- 
ed by mammalian Remains from two middle Patago- 
nian localities, both Late Cretaceous in age (Los 
mammal history Is ra(hcally divided into two major Alamitos and La Colonia, Chubut; Fig. 4). Both 
and unrehiled episodes occinrlng under two distinct Patagonian Late Cretaceous mammal asseml)higes 

(apparently Cam])anian) are comprised only of non- 
tribosphenic and pre-lribosj)henic mammals. 

Based on the Patagonian records, and the Bolivian 

geographic: sceneries. Thcs(^ two distinctive episodes 
were separated by a ndafively long Maastriehtian— 

early Paleoeene hiatus; there is only one dubious early 

Paleoeene Patagotiian s[)ecimcn, a tribosphenic molar one (Patidia Pata) nKMitionerl above (if the sui^posed 

found (pule recently (Coin el al., 2005). This molar euthc^rian Is really of Condwanan origin), fhe 

may well represent one of the oldest therians to have Gondw^anan Episode extended from the latest Creta- 

emigt-ated from Latn-asia. emlxxlying the begimiing of ceous (Caitipanian) lo earliest Paleoeene (Daman) 

The South Am<MMcan Episode. Additionally, an interval, and thus far is rej)resented only In these two 

assembhige from Pxdivia, of midehe Maastriehtian central Patagonian localities, and probal)ly Bolivia. 

age based on inlerbeddcd marine 

taxa, includes an Similar slratlgrapliic seciuenees and land mannnal 


Annals of the 

Missouri Botanical Garden 








^ ^ 












lM<iuiv .1.1. A roin|)ari>(iii of ri^lil di-nlnrics in (a) hil>ial. (h) liiifjiiaL and (r| nccliisal \icws of (A) llic rarlv I'alnicrMC 
Condnaiialhcria Siidtuumra iiiiii'gliuiiii Si illalo Yaiir ^K Pa.sciial. 1984 uilli I lij tlie [.ale Miixnii- cav iotiiotpli iddciil 
Diiiornyidar Telnislyliis Amfgliino, 1886 sp. Scale bais: 1 cm. iMi^urv ,'5.2. A ciiiipari^-on of llic hi.iiKildjioiis Icfl ml of llu; 
Gondwaiiallici-lans (A) lu-ni^li,,lhrriniu icindliiiusrni ISonaparU!, (li) CondiraiKillicriiini jxilnixunicuin ISonapailc, and (C) 
Sudiiincriid nme^liiiKii \\\\\\ llic laic Mioi'cnc cavioniorpli rndrni Dinninxidac (D) l'ent(istdnm\s Kra<j;lic\ icii. 1926. Scale bars: 

gni(M-a present al luUli rata^^oiiiaii localities indicate (IiiIhoiis Laiirasian TricoiKMlojita, Svinnielrodoiila. and 

syncliriHiicity, representing continetital faeies of 

Docodonta. plus an arra) of quile advanctnl Dryoles- 

a wide-ranging (^[U'irogcMiie marine Canipanian-Oa- loidca (Figs. :^. 6). Tlie record of ihe liolivian 
nian Iransgression (Bonaparte, 1987a, 19871), 1996; Maaslrielilian Kutlierian (see al 

)o\(M may mdicate 

Pascual et al., 2()t)()a; Fig. 4). Tins transgression tlial this is nol a valid generall/alion for llie \vh(»le 

exlended along the lengtli of tlu^ eastern region of die cofitlnenl. and dial l^itagonia — as insinuated \)\ some 
Andes, as far as (he 

Bolivian Fake 'rilicaca. During 

oilier fossil \ertelnates (si;e belou) — itiay Ik 
the Campanian a coelaneon.^ "Carihltean" Iransirres- 

sion eoimeeted U) the rorincr hy the 7'iticaea region. second half of the Me^.o/oic to the PrescnI. I 

i\e ha( 

which, as a seawav. di\ ided die Soulh A 


a distinct hiogeograpliic hislorv, at least IVoiii the 

n an\ 

case, diis does \m)\ refute the exisU^nce of the t 


territory into two Fate (a-elaeeoiis-early Paleocctie th^tinct major cpisotles dial characUa'i/ed the Soull 
terrestrial hlogeographit-al pr(»\inc-(^s (^^pro\incc iiord- Atnetican land mafnmal history. 

gondwanlenne" ami "pro\ ince ftiid-i;()ndwaiii<-nne," 

Honapart(= (F)o(>) discovered an l\arl> Cretaceous 
sensu Ih-oin & de la Fuente, 1 99:5), v(a-ified hy various mammal Vincclcsies nciujucnidiius Ronaparic, from 

ahiolic and l)i(.[ie evidences (Wilson & Arens, 2001: another norlh weslern l*alagouiaii locality (Fig. 3), 
Fi" 11 1 

liich he considered lo he EupaiitothtMian. T 

The Palagouian Fate Cretaceous record (the ino^l Bonaparte and Ih.ugier (1987). Butler (1990J, and 

iuformalive and <do(ineully repre